P2 receptor-mediated modulation of neurotransmitter release - An update

Purinergic Signalling

Volumn 3, Issue 4, 2007, Pages 269-284

  Sperlágh, Beáta ^a   Heinrich, Attila ^a   Csölle, Cecilia ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Neuromodulation; P2X receptor; P2Y receptors; Presynaptic; Release; Transmitter

Indexed keywords

EID: 36248948480     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-007-9080-0     Document Type: Review

References (207)

1. Boehm S, Kubista H (2002) Fine tuning of sympathetic transmitter release via ionotropic and metabotropic presynaptic receptors. Pharmacol Rev 54:43-99
2. McGehee DS, Role LW (1996) Presynaptic ionotropic receptors. Curr Opin Neurobiol 6:342-349
3. Vizi ES (2000) Role of high-affinity receptors and membrane transporters in nonsynaptic communication and drug action in the central nervous system. Pharmacol Rev 52:63-89
4. MacDermott AB, Role LW, Siegelbaum SA (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485
5. von Kugelgen I, Schoffel E, Starke K (1989) Inhibition by nucleotides acting at presynaptic P2-receptors of sympathetic neuro-effector transmission in the mouse isolated vas deferens. Naunyn Schmiedebergs Arch Pharmacol 340:522-532
6. Sperlagh B, Vizi ES (1991) Effect of presynaptic P2 receptor stimulation on transmitter release. J Neurochem 56:1466-1470
7. Cunha RA, Ribeiro JA (2000) ATP as a presynaptic modulator. Life Sci 68:119-137
8. Sperlágh B, Vizi ES (1996) Neuronal synthesis, storage and release of ATP. Semin Neurosci 8:175-186
9. Sperlagh B, Vizi ES (2000) Regulation of purine release. In: Abbracchio MP, Williams M (eds) Handbook of experimental pharmacology, vol 151. Springer, Berlin, pp 179-209
10. Cunha RA, Vizi ES, Ribeiro JA et al (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
11. Sperlagh B, Kittel A, Lajtha A et al (1995) ATP acts as fast neurotransmitter in rat habenula: Neurochemical and enzymecytochemical evidence. Neuroscience 66:915-920
12. Wieraszko A, Goldsmith G, Seyfried TN (1989) Stimulation-dependent release of adenosine triphosphate from hippocampal slices. Brain Res 485:244-250
13. Braun N, Sevigny J, Robson SC et al (2000) Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain. Eur J Neurosci 12:4357-4366
14. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362:299-309
15. Coco S, Calegari F, Pravettoni E et al (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354-1362
16. 7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821-827
17. Verderio C, Matteoli M (2001) ATP mediates calcium signaling between astrocytes and microglial cells: Modulation by IFN-gamma. J Immunol 166:6383-6391
18. Gourine AV, Llaudet E, Dale N et al (2005) ATP is a mediator of chemosensory transduction in the central nervous system. Nature 436:108-111
19. Wang Y, Roman R, Lidofsky SD et al (1996) Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc Natl Acad Sci U S A 93:12020-12025
20. Melani A, Turchi D, Vannucchi MG et al (2005) ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem Int 47:442-448
21. Lutz PL, Kabler S (1997) Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Res 769:281-286
22. 3 H]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices. Brain Res 823:183-190
23. Hisanaga K, Onodera H, Kogure K (1986) Changes in levels of purine and pyrimidine nucleotides during acute hypoxia and recovery in neonatal rat brain. J Neurochem 47:1344-1350
24. Frenguelli BG, Wigmore G, Llaudet E et al (2007) Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J Neurochem 101:1400-1413
25. Gourine AV, Llaudet E, Dale N et al (2005) Release of ATP in the ventral medulla during hypoxia in rats: Role in hypoxic ventilatory response. J Neurosci 25:1211-1218
26. Ferrari D, Chiozzi P, Falzoni S et al (1997) Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med 185:579-582
27. 7 receptors. Neurochem Int 33:209-215
28. Sperlagh B, Baranyi M, Hasko G et al (2004) Potent effect of interleukin-1 beta to evoke ATP and adenosine release from rat hippocampal slices. J Neuroimmunol 151:33-39
29. Sperlagh B, Szabo G, Erdelyi F et al (2003) Homo- and heteroexchange of adenine nucleotides and nucleosides in rat hippocampal slices by the nucleoside transport system. Br J Pharmacol 139:623-633
30. Latini S, Pedata F (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neurochem 79:463-484
31. Pearson RA, Dale N, Llaudet E et al (2005) ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46:731-744
32. Zhang X, Chen Y, Wang C et al (2007) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci U S A 104:9864-9869
33. Schwiebert EM (1999) ABC transporter-facilitated ATP conductive transport. Am J Physiol 276:C1-C8
34. al-Awqati Q (1995) Regulation of ion channels by ABC transporters that secrete ATP. Science 269:805-806
35. Ballerini P, Di Iorio P, Ciccarelli R et al (2002) Glial cells express multiple ATP binding cassette proteins which are involved in ATP release. Neuroreport 13:1789-1792
36. Abdipranoto A, Liu GJ, Werry EL et al (2003) Mechanisms of secretion of ATP from cortical astrocytes triggered by uridine triphosphate. Neuroreport 14:2177-2181
37. Darby M, Kuzmiski JB, Panenka W et al (2003) ATP released from astrocytes during swelling activates chloride channels. J Neurophysiol 89:1870-1877
38. Stout C, Goodenough DA, Paul DL (2004) Connexins: Functions without junctions. Curr Opin Cell Biol 16:507-512
39. Stout CE, Costantin JL, Naus CC et al (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488
40. Gomes P, Srinivas SP, Van Driessche W et al (2005) ATP release through connexin hemichannels in corneal endothelial cells. Invest Ophthalmol Vis Sci 46:1208-1218
41. Braet K, Vandamme W, Martin PE et al (2003) Photoliberating inositol-1,4,5-trisphosphate triggers ATP release that is blocked by the connexin mimetic peptide gap 26. Cell Calcium 33:37-48
42. Cook SP, McCleskey EW (2002) Cell damage excites nociceptors through release of cytosolic ATP. Pain 95:41-47
43. Wang TF, Rosenberg PA, Guidotti G (1997) Characterization of brain ecto-apyrase: Evidence for only one ecto-apyrase (CD39) gene. Brain Res Mol Brain Res 47:295-302
44. Wang TF, Guidotti G (1998) Widespread expression of ecto-apyrase (CD39) in the central nervous system. Brain Res 790:318-322
45. Cunha RA, Sebastiao 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
46. 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
47. 3 H]acetylcholine from the hippocampus and cerebral cortex of the rat: Role of the ectonucleotidases. Eur J Neurosci 6:33-42
48. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165-174
49. Valera S, Hussy N, Evans RJ et al (1994) A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATP. Nature 371:516-519
50. North RA, Surprenant A (2000) Pharmacology of cloned P2X receptors. Annu Rev Pharmacol Toxicol 40:563-580
51. Torres GE, Egan TM, Voigt MM (1999) Hetero-oligomeric assembly of P2X receptor subunits. Specificities exist with regard to possible partners. J Biol Chem 274:6653-6659
52. 6 receptors by N-linked glycosylation: Identification of a novel alpha beta-methylene ATP-sensitive phenotype. Mol Pharmacol 65:979-985
53. Gever JR, Cockayne DA, Dillon MP et al (2006) Pharmacology of P2X channels. Pflugers Arch 452:513-537
54. 4 subunits. J Neurochem 92:925-933
55. 6 channel subunits coassemble into a novel heteromeric ATP receptor. J Neurosci 18:7152-7159
56. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377:432-435
57. Brown SG, Townsend-Nicholson A, Jacobson KA et al (2002) Heteromultimeric P2X(1/2) receptors show a novel sensitivity to extracellular pH. J Pharmacol Exp Ther 300:673-680
58. 6 subunits in Xenopus oocytes. J Neurosci 20:4871-4877
59. 5 receptor subunits reveals a novel ATP-gated ion channel. Mol Pharmacol 54:989-993
60. 6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16:2495-2507
61. Atkinson L, Batten TF, Deuchars J (2000) P2X2 receptor immunoreactivity in the dorsal vagal complex and area postrema of the rat. Neuroscience 99:683-696
62. Rubio M, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641-653
63. Vulchanova L, Arvidsson U, Riedl M et al (1996) Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc Natl Acad Sci U S A 93:8063-8067
64. 2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407:11-32
65. 3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36:1229-1242
66. 1 receptors revealed using knockout mice. Mol Pharmacol 65:139-148
67. 3 receptors. Pflugers Arch 450:381-389
68. Papp L, Balazsa T, Kofalvi A et al (2004) P2X receptor activation elicits transporter-mediated noradrenaline release from rat hippocampal slices. J Pharmacol Exp Ther 310:973-980
69. 4 receptors in the rat hippocampus. J Neurosci 25:6286-6295
70. Le KT, Paquet M, Nouel D et al (1997) Primary structure and expression of a naturally truncated human P2X ATP receptor subunit from brain and immune system. FEBS Lett 418:195-199
71. Yao ST, Barden JA, Lawrence AJ (2001) On the immunohistochemical distribution of ionotropic P2X receptors in the nucleus tractus solitarius of the rat. Neuroscience 108:673-685
72. 7 receptor. Neuropharmacology 36:1277-1283
73. 7 receptor subunit with vesicular glutamate transporters VGLUT1 and VGLUT2 in rat CNS. Neuroscience 123:761-768
74. 7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143-7152
75. 7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J Neurochem 81:1196-1211
76. 7 receptor expression in rodent brain. J Neurosci 24:6307-6314
77. 7 receptor agonist 2′-3′-O-(4-benzoylbenzoyl)-ATP. J Neurosci 24:7128-7139
78. Sanchez-Nogueiro J, Marin-Garcia P, Miras-Portugal MT (2005) Characterization of a functional P2X 7 -like receptor in cerebellar granule neurons from P2X 7 knockout mice. FEBS Lett 579:3783-3788
79. 14 receptor) adds diversity to the P2Y receptor family. Trends Pharmacol Sci 24:52-55
80. Barnard EA, Simon J (2001) An elusive receptor is finally caught: P2Y(12′), an important drug target in platelets. Trends Pharmacol Sci 22:388-391
81. Communi D, Gonzalez NS, Detheux M et al (2001) Identification of a novel human ADP receptor coupled to G(i). J Biol Chem 276:41479-41485
82. von Kugelgen I, Wetter A (2000) Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch Pharmacol 362:310-323
83. Abbracchio MP, Burnstock G, Boeynaems JM et al (2006) International Union of Pharmacology LVIII: Update on the P2Y G protein-coupled nucleotide receptors: From molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281-341
84. von Kugelgen I (2006) Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol Ther 110:415-432
85. Hussl S, Boehm S (2006) Functions of neuronal P2Y receptors. Pflugers Arch 452:538-551
86. Yoshioka K, Saitoh O, Nakata H (2001) Heteromeric association creates a P2Y-like adenosine receptor. Proc Natl Acad Sci U S A 98:7617-7622
87. Chambers JK, Macdonald LE, Sarau HM et al (2000) A G protein-coupled receptor for UDP-glucose. J Biol Chem 275:10767-10771
88. Hollopeter G, Jantzen HM, Vincent D et al (2001) Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 409:202-207
89. 12 receptor: A novel member of the P2Y family of receptors activated by extracellular nucleotides. Mol Pharmacol 60:416-420
90. Moore DJ, Chambers JK, Wahlin JP et al (2001) Expression pattern of human P2Y receptor subtypes: A quantitative reverse transcription-polymerase chain reaction study. Biochim Biophys Acta 1521:107-119
91. Moran-Jimenez MJ, Matute C (2000) Immunohistochemical localization of the P2Y1 purinergic receptor in neurons and glial cells of the central nervous system. Brain Res Mol Brain Res 78:50-58
92. Franke H, Krugel U, Grosche J et al (2004) P2Y receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 127:431-441
93. Zhu Y, Kimelberg HK (2004) Cellular expression of P2Y and beta-AR receptor mRNAs and proteins in freshly isolated astrocytes and tissue sections from the CA1 region of P8-12 rat hippocampus. Brain Res 148:77-87
94. 2 receptor mRNA in the cerebellum. Methods Mol Biol (Clifton, NJ) 326:151-162
95. Sergeeva OA, Klyuch BP, Fleischer W et al (2006) P2Y receptor-mediated excitation in the posterior hypothalamus. Eur J Neurosci 24:1413-1426
96. 6 and atypical UTP-sensitive receptors coupled to rises in intracellular calcium in mouse cultured superior cervical ganglion neurons and glia. Br J Pharmacol 143:525-532
97. 13 receptor. Biochem Pharmacol 68:113-124
98. Moore DJ, Murdock PR, Watson JM et al (2003) GPR105, a novel Gi/ o-coupled UDP-glucose receptor expressed on brain glia and peripheral immune cells, is regulated by immunologic challenge: Possible role in neuroimmune function. Brain Res 118:10-23
99. 12 metabotropic receptor in adult rat brain. Neuroscience 141:1171-1180
100. 12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512-1519
101. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31-304
102. Egan TM, Khakh BS (2004) Contribution of calcium ions to P2X channel responses. J Neurosci 24:3413-3420
103. Rogers M, Colquhoun LM, Patrick JW et al (1997) Calcium flux through predominantly independent purinergic ATP and nicotinic acetylcholine receptors. J Neurophysiol 77:1407-1417
104. Fu WM, Poo MM (1991) ATP potentiates spontaneous transmitter release at developing neuromuscular synapses. Neuron 6:837-843
105. Sun XP, Stanley EF (1996) An ATP-activated, ligand-gated ion channel on a cholinergic presynaptic nerve terminal. Proc Natl Acad Sci U S A 93:1859-1863
106. Hong SJ, Chang CC (1998) Evaluation of intrinsic modulation of synaptic transmission by ATP in mouse fast twitch muscle. J Neurophysiol 80:2550-2558
107. Fu WM, Chen YH, Lee KF et al (1997) Regulation of quantal transmitter secretion by ATP and protein kinases at developing neuromuscular synapses. Eur J Neurosci 9:676-685
108. Salgado AI, Cunha RA, Ribeiro JA (2000) Facilitation by P2 receptor activation of acetylcholine release from rat motor nerve terminals: interaction with presynaptic nicotinic receptors. Brain Res 877:245-250
109. 7 -like receptors at the neuromuscular junction. Brain Res 1034:40-50
110. Miyahara H, Suzuki H (1987) Pre- and post-junctional effects of adenosine triphosphate on noradrenergic transmission in the rabbit ear artery. J Physiol 389:423-440
111. Inoue K, Nakazawa K, Fujimori K et al (1989) Extracellular adenosine 5′-triphosphate-evoked norepinephrine secretion not relating to voltage-gated Ca channels in pheochromocytoma PC12 cells. Neurosci Lett 106:294-299
112. Arthur DB, Taupenot L, Insel PA (2007) Nerve growth factor-stimulated neuronal differentiation induces changes in P2 receptor expression and nucleotide-stimulated catecholamine release. J Neurochem 100:1257-1264
113. Queiroz G, Talaia C, Goncalves J (2003) ATP modulates noradrenaline release by activation of inhibitory P2Y receptors and facilitatory P2X receptors in the rat vas deferens. J Pharmacol Exp Ther 307:809-815
114. Sesti C, Broekman MJ, Drosopoulos JH et al (2002) EctoNucleotidase in cardiac sympathetic nerve endings modulates ATP-mediated feedback of norepinephrine release. J Pharmacol Exp Ther 300:605-611
115. 3 H]-noradrenaline release from the isolated guinea-pig right atrium by P2X-receptors located on axon terminals. Br J Pharmacol 131:1775-1783
116. Boehm S (1999) ATP stimulates sympathetic transmitter release via presynaptic P2X purinoceptors. J Neurosci 19:737-746
117. Norenberg W, Gobel I, Meyer A et al (2001) Stimulation of mouse cultured sympathetic neurons by uracil but not adenine nucleotides. Neuroscience 103:227-236
118. Sesti C, Koyama M, Broekman MJ et al (2003) Ectonucleotidase in sympathetic nerve endings modulates ATP and norepinephrine exocytosis in myocardial ischemia. J Pharmacol Exp Ther 306:238-244
119. Machida T, Heerdt PM, Reid AC et al (2005) Ectonucleoside triphosphate diphosphohydrolase 1/CD39, localized in neurons of human and porcine heart, modulates ATP-induced norepinephrine exocytosis. J Pharmacol Exp Ther 313:570-577
120. Frohlich R, Boehm S, Illes P (1996) Pharmacological characterization of P2 purinoceptor types in rat locus coeruleus neurons. Eur J Pharmacol 315:255-261
121. Okada M, Kawata Y, Murakami T et al (1999) Interaction between purinoceptor subtypes on hippocampal serotonergic transmission using in vivo microdialysis. Neuropharmacology 38:707-715
122. Zhang YX, Yamashita H, Ohshita T et al (1996) ATP induces release of newly synthesized dopamine in the rat striatum. Neurochem Int 28:395-400
123. Zhang YX, Yamashita H, Ohshita T et al (1995) ATP increases extracellular dopamine level through stimulation of P2Y purinoceptors in the rat striatum. Brain Res 691:205-212
124. Krugel U, Kittner H, Illes P (1999) Adenosine 5′-triphosphate-induced dopamine release in the rat nucleus accumbens in vivo. Neurosci Lett 265:49-52
125. Krugel U, Kittner H, Illes P (2001) Mechanisms of adenosine 5′-triphosphate-induced dopamine release in the rat nucleus accumbens in vivo. Synapse 39:222-232
126. Krugel U, Kittner H, Franke H et al (2003) Purinergic modulation of neuronal activity in the mesolimbic dopaminergic system in vivo. Synapse 47:134-142
127. Kittner H, Krugel U, El-Ashmawy IM et al (2000) Suppression of feeding-evoked dopamine release in the rat nucleus accumbens by the blockade of P2 purinoceptors. Eur J Pharmacol 406:R13-R14
128. Kittner H, Krugel U, Hoffmann E et al (2004) Modulation of feeding behaviour by blocking purinergic receptors in the rat nucleus accumbens: a combined microdialysis, electroencephalographic and behavioural study. Eur J Neurosci 19:396-404
129. Jin YH, Bailey TW, Li BY et al (2004) Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. J Neurosci 24:4709-4717
130. Kato F, Shigetomi E (2001) Distinct modulation of evoked and spontaneous EPSCs by purinoceptors in the nucleus tractus solitarii of the rat. J Physiol 530:469-486
131. Khakh BS, Henderson G (1998) ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol Pharmacol 54:372-378
132. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network. J Neurosci 24:3125-3135
133. Khakh BS, Gittermann D, Cockayne DA et al (2003) ATP modulation of excitatory synapses onto interneurons. J Neurosci 23:7426-7437
134. Fellin T, Pozzan T, Carmignoto G (2006) Purinergic receptors mediate two distinct glutamate release pathways in hippocampal astrocytes. J Biol Chem 281:4274-4284
135. Inoue K, Nakazawa K, Fujimori K et al (1992) Extracellular adenosine 5′-triphosphate-evoked glutamate release in cultured hippocampal neurons. Neurosci Lett 134:215-218
136. Patti L, Raiteri L, Grilli M et al (2006) P2X7 receptors exert a permissive role on the activation of release-enhancing presynaptic alpha7 nicotinic receptors co-existing on rat neocortex glutamatergic terminals. Neuropharmacology 50:705-713
137. 7 receptor -/- mice. Neuroreport 15:2387-2391
138. 7 receptor subtypes. Br J Pharmacol 135:1616-1626
139. 7 receptors in rat brain: Presence in synaptic terminals and granule cells. Neurochem Res 28:1597-1605
140. Papp L, Vizi ES, Sperlagh B (2007) P2X 7 receptor mediated phosphorylation of p38MAP kinase in the hippocampus. Biochem Biophys Res Commun 355:568-574
141. 7 -like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase. J Neurosci 22:5938-5945
142. 7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320-1328
143. 7 receptors in Müller glial cells from the human retina. J Neurosci 20:5965-5972
144. Nakatsuka T, Tsuzuki K, Ling JX et al (2003) Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord. J Neurophysiol 89:3243-3252
145. Nakatsuka T, Gu JG (2001) ATP P2X receptor-mediated enhancement of glutamate release and evoked EPSCs in dorsal horn neurons of the rat spinal cord. J Neurosci 21:6522-6531
146. Gu JG, MacDermott AB (1997) Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389:749-753
147. Li J, Perl ER (1995) ATP modulation of synaptic transmission in the spinal substantia gelatinosa. J Neurosci 15:3357-3365
148. Li P, Calejesan AA, Zhuo M (1998) ATP P2X receptors and sensory synaptic transmission between primary afferent fibers and spinal dorsal horn neurons in rats. J Neurophysiol 80:3356-3360
149. Krugel U, Schraft T, Regenthal R et al (2004) Purinergic modulation of extracellular glutamate levels in the nucleus accumbens in vivo. Int J Dev Neurosci 22:565-570
150. Price GD, Robertson SJ, Edwards FA (2003) Long-term potentiation of glutamatergic synaptic transmission induced by activation of presynaptic P2Y receptors in the rat medial habenula nucleus. Eur J Neurosci 17:844-850
151. 1 receptor-evoked glutamate exocytosis from astrocytes: Control by tumor necrosis factor-alpha and prostaglandins. J Biol Chem 281:30684-30696
152. Jeftinija SD, Jeftinija KV (1998) ATP stimulates release of excitatory amino acids from cultured Schwann cells. Neuroscience 82:927-934
153. Gomez-Villafuertes R, Gualix J, Miras-Portugal MT (2001) Single GABAergic synaptic terminals from rat midbrain exhibit functional P2X and dinucleotide receptors able to induce GABA secretion. J Neurochem 77:84-93
154. Hugel S, Schlichter R (2000) Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J Neurosci 20:2121-2130
155. Wirkner K, Kofalvi A, Fischer W et al (2005) Supersensitivity of P2X receptors in cerebrocortical cell cultures after in vitro ischemia. J Neurochem 95:1421-1437
156. Inoue K, Koizumi S, Ueno S et al (1999) The functions of ATP receptors in the synaptic transmission in the hippocampus. Prog Brain Res 120:193-206
157. Watano T, Calvert JA, Vial C et al (2004) P2X receptor subtype-specific modulation of excitatory and inhibitory synaptic inputs in the rat brainstem. J Physiol 558:745-757
158. Aihara H, Fujiwara S, Mizuta I et al (2002) Adenosine triphosphate accelerates recovery from hypoxic/hypoglycemic perturbation of guinea pig hippocampal neurotransmission via a P2 receptor. Brain Res 952:31-37
159. - -dependent mechanism. Glia 37:8-18
160. 3 H]GABA release from rat hippocampal nerve terminals. Neuropharmacology 39:1156-1167
161. Rhee JS, Wang ZM, Nabekura J et al (2000) ATP facilitates spontaneous glycinergic IPSC frequency at dissociated rat dorsal horn interneuron synapses. J Physiol 524(Pt 2):471-483
162. Wang ZM, Katsurabayashi S, Rhee JS et al (2001) Substance P abolishes the facilitatory effect of ATP on spontaneous glycine release in neurons of the trigeminal nucleus pars caudalis. J Neurosci 21:2983-2991
163. Kawamura M, Gachet C, Inoue K et al (2004) Direct excitation of inhibitory interneurons by extracellular ATP mediated by P2Y1 receptors in the hippocampal slice. J Neurosci 24:10835-10845
164. Vizi ES, Knoll J (1976) The inhibitory effect of adenosine and related nucleotides on the release of acetylcholine. Neuroscience 1:391-398
165. Silinsky EM, Ginsborg BL (1983) Inhibition of acetylcholine release from preganglionic frog nerves by ATP but not adenosine. Nature 305:327-328
166. Wiklund NP, Gustafsson LE, Lundin J (1985) Pre- and postjunctional modulation of cholinergic neuroeffector transmission by adenine nucleotides. Experiments with agonists and antagonists. Acta Physiol Scand 125:681-691
167. Wiklund NP, Gustafsson LE (1986) Neuromodulation by adenine nucleotides, as indicated by experiments with inhibitors of nucleotide inactivation. Acta Physiol Scand 126:217-223
168. Reese JH, Cooper JR (1982) Modulation of the release of acetylcholine from ileal synaptosomes by adenosine and adenosine 5′-triphosphate. J Pharmacol Exp Ther 223:612-616
169. Barajas-Lopez C, Muller MJ, Prieto-Gomez B et al (1995) ATP inhibits the synaptic release of acetylcholine in submucosal neurons. J Pharmacol Exp Ther 274:1238-1245
170. Giniatullin RA, Sokolova EM (1998) ATP and adenosine inhibit transmitter release at the frog neuromuscular junction through distinct presynaptic receptors. Br J Pharmacol 124:839-844
171. Smith AB, Hansen MA, Liu DM et al (2001) Pre- and postsynaptic actions of ATP on neurotransmission in rat submandibular ganglia. Neuroscience 107:283-291
172. Neal M, Cunningham J (1994) Modulation by endogenous ATP of the light-evoked release of ACh from retinal cholinergic neurones. Br J Pharmacol 113:1085-1087
173. De Lorenzo S, Veggetti M, Muchnik S et al (2006) Presynaptic inhibition of spontaneous acetylcholine release mediated by P2Y receptors at the mouse neuromuscular junction. Neuroscience 142:71-85
174. Stjarne L, Astrand P (1985) Relative pre- and postjunctional roles of noradrenaline and adenosine 5′-triphosphate as neurotransmitters of the sympathetic nerves of guinea-pig and mouse vas deferens. Neuroscience 14:929-946
175. Fujioka M, Cheung DW (1987) Autoregulation of neuromuscular transmission in the guinea-pig saphenous artery. Eur J Pharmacol 139:147-153
176. Shinozuka K, Bjur RA, Westfall DP (1988) Characterization of prejunctional purinoceptors on adrenergic nerves of the rat caudal artery. Naunyn Schmiedebergs Arch Pharmacol 338:221-227
177. Shinozuka K, Bjur RA, Westfall DP (1990) Effects of alpha,beta-methylene ATP on the prejunctional purinoceptors of the sympathetic nerves of the rat caudal artery. J Pharmacol Exp Ther 254:900-904
178. Forsyth KM, Bjur RA, Westfall DP (1991) Nucleotide modulation of norepinephrine release from sympathetic nerves in the rat vas deferens. J Pharmacol Exp Ther 256:821-826
179. von Kugelgen I, Kurz K, Starke K (1993) Axon terminal P2-purinoceptors in feedback control of sympathetic transmitter release. Neuroscience 56:263-267
180. Goncalves J, Queiroz G (1996) Purinoceptor modulation of noradrenaline release in rat tail artery: Tonic modulation mediated by inhibitory P2Y- and facilitatory A2A-purinoceptors. Br J Pharmacol 117:156-160
181. von Kugelgen I, Kurz K, Starke K (1994) P2-purinoceptor-mediated autoinhibition of sympathetic transmitter release in mouse and rat vas deferens. Naunyn Schmiedebergs Arch Pharmacol 349:125-132
182. Kurz K, von Kugelgen I, Starke K (1993) Prejunctional modulation of noradrenaline release in mouse and rat vas deferens: Contribution of P1- and P2-purinoceptors. Br J Pharmacol 110:1465-1472
183. von Kugelgen I, Stoffel D, Starke K (1995) P2-purinoceptor-mediated inhibition of noradrenaline release in rat atria. Br J Pharmacol 115:247-254
184. Fuder H, Muth U (1993) ATP and endogenous agonists inhibit evoked [3 H]-noradrenaline release in rat iris via A1 and P2y-like purinoceptors. Naunyn Schmiedebergs Arch Pharmacol 348:352-357
185. Bohmann C, von Kugelgen I, Rump LC (1997) P2-receptor modulation of noradrenergic neurotransmission in rat kidney. Br J Pharmacol 121:1255-1262
186. Koch H, von Kugelgen I, Starke K (1998) P2-receptor-mediated inhibition of noradrenaline release in the rat pancreas. Naunyn Schmiedebergs Arch Pharmacol 357:431-440
187. Allgaier C, Wellmann H, Schobert A et al (1995) Cultured chick sympathetic neurons: Modulation of electrically evoked noradrenaline release by P2-purinoceptors. Naunyn Schmiedebergs Arch Pharmacol 352:17-24
188. Allgaier C, Pullmann F, Schobert A et al (1994) P2 purinoceptors modulating noradrenaline release from sympathetic neurons in culture. Eur J Pharmacol 252:R7-R8
189. 2+ channels. Eur J Neurosci 20:2917-2928
190. 12 receptor in nucleotide inhibition of exocytosis from bovine chromaffin cells. Mol Pharmacol 66:601-611
191. Trendelenburg AU, Cox SL, Gaiser EG et al (1999) Noradrenaline release from cultured mouse postganglionic sympathetic neurons: autoreceptor-mediated modulation. J Neurochem 73:1439-1445
192. 2+ -ATPases in the capsule-glomerulosa fraction of the rat adrenal gland. J Endocrinol 153:105-114
193. O'Connor SC, Brain KL, Bennett MR (1999) Individual sympathetic varicosities possess different sensitivities to alpha 2 and P2 receptor agonists and antagonists in mouse vas deferens. Br J Pharmacol 128:1739-1753
194. Powell AD, Taschenmacher AG, Seward EP (2000) P2Y purinoceptors inhibit exocytosis in adrenal chromaffin cells via modulation of voltage-operated calcium channels. J Neurosci 20:606-616
195. von Kugelgen I, Spath L, Starke K (1994) Evidence for P2-purinoceptor-mediated inhibition of noradrenaline release in rat brain cortex. Br J Pharmacol 113:815-822
196. Koch H, von Kugelgen I, Starke K (1997) P2-receptor-mediated inhibition of noradrenaline release in the rat hippocampus. Naunyn Schmiedebergs Arch Pharmacol 355:707-715
197. von Kugelgen I, Koch H, Starke K (1997) P2-receptor-mediated inhibition of serotonin release in the rat brain cortex. Neuropharmacology 36:1221-1227
198. Trendelenburg AU, Bultmann R (2000) P2 receptor-mediated inhibition of dopamine release in rat neostriatum. Neuroscience 96:249-252
199. Bennett GC, Boarder MR (2000) The effect of nucleotides and adenosine on stimulus-evoked glutamate release from rat brain cortical slices. Br J Pharmacol 131:617-623
200. 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
201. Masino SA, Diao L, Illes P et al (2002) Modulation of hippocampal glutamatergic transmission by ATP is dependent on adenosine A1 receptors. J Pharmacol Exp Ther 303:356-363
202. 2+ channels in rat dorsal root ganglion neurons. Synapse 47:159-161
203. Illes P, Gerevich Z (2004) P2Y receptor and pain transmission. Purinergic Signalling 1:3-10
204. Gerevich Z, Borvendeg SJ, Schroder W et al (2004) Inhibition of N-type voltage-activated calcium channels in rat dorsal root ganglion neurons by P2Y receptors is a possible mechanism of ADP-induced analgesia. J Neurosci 24:797-807
205. Koizumi S, Fujishita K, Tsuda M et al (2003) Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc Natl Acad Sci U S A 100:11023-11028
206. Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606-8620
207. Sperlágh B, Zsilla G, Baranyi M et al Purinergic modulation of glutamate release under ischemic-like conditions in the hippocampus. Neuroscience (in press)