Ionotropic ATP receptors in neuronal-glial communication

Seminars in Cell and Developmental Biology

Volumn 22, Issue 2, 2011, Pages 220-228

  Lalo, Ulyana ^a   Verkhratsky, Alexei ^b   Pankratov, Yuri ^c  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

ATP release; Neuroglia; Neuronal glial interactions; P2X receptors; Purinoceptors

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ADENOSINE TRIPHOSPHATE; CALCIUM ION; GLUTAMIC ACID; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; SODIUM ION;

ASTROCYTE; BRAIN CORTEX; CELL COMMUNICATION; CELL METABOLISM; CELL MIGRATION; CYTOPLASM; ION CURRENT; MOLECULAR MECHANICS; NERVE CELL; NERVE ENDING; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 79953189641     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.02.012     Document Type: Review

References (114)

1. Burnstock G., Fredholm B.B., North R.A., Verkhratsky A. The birth and postnatal development of purinergic signalling. Acta Physiol (Oxf) 2010, 199:93-147.
2. Clark G., Roux S.J. Extracellular nucleotides: ancient signaling molecules. Plant Sci 2009, 177:239-244.
3. Burnstock G., Verkhratsky A. Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis 2010, 1:e9.
4. Di Virgilio F., Ceruti S., Bramanti P., Abbracchio M.P. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci 2009, 32:79-87.
5. North R.A. Molecular physiology of P2X receptors. Physiol Rev 2002, 82:1013-1067.
6. Surprenant A., North R.A. Signaling at purinergic P2X receptors. Annu Rev Physiol 2009, 71:333-359.
7. Verkhratsky A., Krishtal O.A., Burnstock G. Purinoceptors on neuroglia. Mol Neurobiol 2009, 39:190-208.
8. Abbracchio M.P., Burnstock G., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., et al. International Union of Pharmacology. LVIII: Update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 2006, 58:281-341.
9. Fredholm B.B.I.J.A.P., Jacobson K.A., Klotz K.N., Linden J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 2001, 53:527-552.
10. Boison D., Chen J.F., Fredholm B.B. Adenosine signaling and function in glial cells. Cell Death Differ 2010, 17:1071-1082.
11. Edwards F.A., Gibb A.J., Colquhoun D. ATP receptor-mediated synaptic currents in the central nervous system. Nature 1992, 359:144-147.
12. Jo Y.H., Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci 1999, 2:241-245.
13. Pankratov Y., Castro E., Miras-Portugal M.T., Krishtal O. A purinergic component of the excitatory postsynaptic current mediated by P2X receptors in the CA1 neurons of the rat hippocampus. Eur J Neurosci 1998, 10:3898-3902.
14. Pankratov Y., Lalo U., Krishtal O., Verkhratsky A. Ionotropic P2X purinoreceptors mediate synaptic transmission in rat pyramidal neurones of layer II/III of somato-sensory cortex. J Physiol 2002, 542:529-536.
15. Pankratov Y., Lalo U., Krishtal O., Verkhratsky A. P2X receptor-mediated excitatory synaptic currents in somatosensory cortex. Mol Cell Neurosci 2003, 24:842-849.
16. Silinsky E.M., Gerzanich V., Vanner S.M. ATP mediates excitatory synaptic transmission in mammalian neurones. Br J Pharmacol 1992, 106:762-763.
17. Pankratov Y., Lalo U., Krishtal O.A., Verkhratsky A. P2X receptors and synaptic plasticity. Neuroscience 2009, 158:137-148.
18. Lalo U., Pankratov Y., Parpura V., Verkhratsky A. Ionotropic receptors in neuronal-astroglial signalling: what is the role of "excitable" molecules in non-excitable cells. Biochim Biophys Acta 2010, (September). [Epub ahead of print].
19. 4 receptors. Purinergic Signal 2005, 1:95-100.
20. Jarvis M.F. The neural-glial purinergic receptor ensemble in chronic pain states. Trends Neurosci 2010, 33(1):48-57.
21. 2+ signaling. Science 2010, 327:1250-1254.
22. 2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci 2008, 28:4967-4973.
23. Malarkey E.B., Parpura V. Mechanisms of transmitter release from astrocytes. Astrocytes in (patho)physiology of the nervous system 2009, 301-350. Springer, New York. V. Parpura, P.G. Haydon (Eds.).
24. Zhang Z., Chen G., Zhou W., Song A., Xu T., Luo Q., et al. Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 2007, 9:945-953.
25. Scemes E., Suadicani S.O., Dahl G., Spray D.C. Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol 2007, 3:199-208.
26. Liu H.T., Sabirov R.Z., Okada Y. Oxygen-glucose deprivation induces ATP release via maxi-anion channels in astrocytes. Purinergic Signal 2008, 4:147-154.
27. Fields R.D., Ni Y. Nonsynaptic communication through ATP release from volume-activated anion channels in axons. Sci Signal 2010, 3:pra73.
28. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
29. Huang Y.J., Maruyama Y., Dvoryanchikov G., Pereira E., Chaudhari N., Roper S.D. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 2007, 104:6436-6441.
30. Sawada K., Echigo N., Juge N., Miyaji T., Otsuka M., Omote H., et al. Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 2008, 105:5683-5686.
31. Pankratov Y., Lalo U., Verkhratsky A., North R.A. Vesicular release of ATP at central synapses. Pflugers Arch 2006, 452:589-597.
32. Pankratov Y., Lalo U., Verkhratsky A., North R.A. Quantal release of ATP in mouse cortex. J Gen Physiol 2007, 129:257-265.
33. Robertson S.J., Edwards F.A. ATP and glutamate are released from separate neurones in the rat medial habenula nucleus: frequency dependence and adenosine-mediated inhibition of release. J Physiol, Lond 1998, 508:691-701.
34. Burnstock G., Verkhratsky A. Vas deferens - a model used to establish sympathetic cotransmission. Trends Pharmacol Sci 2010, 31:131-139.
35. Jo Y.H., Role L.W. Coordinate release of ATP and GABA at in vitro synapses of lateral hypothalamic neurons. J Neurosci 2002, 22:4794-4804.
36. Mori M., Heuss C., Gahwiler B.H., Gerber U. Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol, Lond 2001, 535:115-123.
37. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., et al. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 1998, 95:15735-15740.
38. Jeremic A., Jeftinija K., Stevanovic J., Glavaski A., Jeftinija S. ATP stimulates calcium-dependent glutamate release from cultured astrocytes. J Neurochem 2001, 77:664-675.
39. Queiroz G., Gebicke-Haerter P.J., Schobert A., Starke K., von Kugelgen I. Release of ATP from cultured rat astrocytes elicited by glutamate receptor activation. Neuroscience 1997, 78:1203-1208.
40. Arcuino G., Lin J.H., Takano T., Liu C., Jiang L., Gao Q., et al. Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci USA 2002, 99:9840-9845.
41. Koizumi S., Fujishita K., Tsuda M., Shigemoto-Mogami Y., Inoue K. Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc Natl Acad Sci USA 2003, 100:11023-11028.
42. Pascual O., Casper K.B., Kubera C., Zhang J., Revilla-Sanchez R., Sul J.Y., et al. Astrocytic purinergic signaling coordinates synaptic networks. Science 2005, 310:113-116.
43. Zhang J.M., Wang H.K., Ye C.Q., Ge W., Chen Y., Jiang Z.L., et al. ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 2003, 40:971-982.
44. Volterra A., Bezzi P. Release of transmitters from glial cells. The tripartite synapse 2002, 164-182. Oxford University Press, Oxford. A. Volterra, P.J. Magistretti, P.G. Haydon (Eds.).
45. Montana V., Ni Y., Sunjara V., Hua X., Parpura V. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 2004, 24:2633-2642.
46. Parpura V, Grubišić V, Verkhratsky A. Ca(2+) sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta (BBA)-Mol Cell Res 2010; Nov 27 [Epub ahead of print].
47. Maienschein V., Marxen M., Volknandt W., Zimmermann H. A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia 1999, 26:233-244.
48. Bal-Price A., Moneer Z., Brown G.C. Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 2002, 40:312-323.
49. Coco S, Calegari F., Pravettoni E., Pozzi D., Taverna E., Rosa P., et al. Storage and release of ATP from astrocytes in culture. J Biol Chem 2003, 278:1354-1362.
50. Pangrsic T., Potokar M., Stenovec M., Kreft M., Fabbretti E., Nistri A., et al. Exocytotic release of ATP from cultured astrocytes. J Biol Chem 2007, 282:28749-28758.
51. Bowser D.N., Khakh B.S. Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 2007, 104:4212-4217.
52. Bowser D.N., Khakh B.S. Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 2007, 129:485-491.
53. Hamilton N.B., Attwell D. Do astrocytes really exocytose neurotransmitters?. Nat Rev Neurosci 2010, 11:227-238.
54. A and NMDA receptors by extracellular ATP: implication for function of tripartite synapse. Biochem Soc Trans 2009, 37:1407-1411.
55. Lalo U., Pankratov Y., Kirchhoff F., North R.A., Verkhratsky A. NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J Neurosci 2006, 26:2673-2683.
56. Shigetomi E., Bowser D.N., Sofroniew M.V., Khakh B.S. Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J Neurosci 2008, 28:6659-6663.
57. Lee C.J., Mannaioni G., Yuan H., Woo D.H., Gingrich M.B., Traynelis S.F. Astrocytic control of synaptic NMDA receptors. J Physiol 2007, 581:1057-1081.
58. Browne L.E., Jiang L.H., North R.A. New structure enlivens interest in P2X receptors. Trends Pharmacol Sci 2010, 31:229-237.
59. 7 heteromeric receptors. Mol Pharmacol 2007, 72:1447-1456.
60. 3 receptor gating near normal body temperature. Pflugers Arch 2008, 456(2):339-347.
61. Lalo U., Verkhratsky A., Pankratov Y. Ivermectin potentiates ATP-induced ion currents in cortical neurones: evidence for functional expression of P2X4 receptors?. Neurosci Lett 2007, 421:158-162.
62. Egan T.M., Khakh B.S. Contribution of calcium ions to P2X channel responses. J Neurosci 2004, 24:3413-3420.
63. Haas S., Brockhaus J., Verkhratsky A., Kettenmann H. ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices. Neuroscience 1996, 75:257-261.
64. Hamilton N., Vayro S., Kirchhoff F., Verkhratsky A., Robbins J., Gorecki D.C., et al. Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 2008, 56:734-749.
65. Todd K.J., Robitaille R. Purinergic modulation of synaptic signalling at the neuromuscular junction. Pflugers Arch 2006, 452:608-614.
66. 7 receptors in the nervous system. Prog Neurobiol 2006, 78:327-346.
67. Jabs R., Matthias K., Grote A., Grauer M., Seifert G., Steinhauser C. Lack of P2X receptor mediated currents in astrocytes and GluR type glial cells of the hippocampal CA1 region. Glia 2007, 55:1648-1655.
68. 5 subunits form the functional P2X receptor in mouse cortical astrocytes. J Neurosci 2008, 28:5473-5480.
69. 2+ signalling in cortical astrocytes. Cell Calcium 2010, 48:225-231.
70. Cockcroft S., Gomperts B.D. ATP induces nucleotide permeability in rat mast cells. Nature 1979, 279:541-542.
71. Rozengurt E., Heppel L.A. A specific effect of external ATP on the permeability of transformed 3T3 cells. Biochem Biophys Res Commun 1975, 67:1581-1588.
72. Gordon J.L. Extracellular ATP: effects, sources and fate. Biochem J 1986, 233:309-319.
73. Di Virgilio F., Ferrari D., Falzoni S., Chiozzi P., Munerati M., Steinberg T.H., et al. P2 purinoceptors in the immune system. Ciba Found Symp 1996, 198:290-302.
74. Pizzo P., Zanovello P., Bronte V., Di Virgilio F. Extracellular ATP causes lysis of mouse thymocytes and activates a plasma membrane ion channel. Biochem J 1991, 274:139-144.
75. 7). Science 1996, 272:735-738.
76. 7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 2008, 132:563-573.
77. 4- receptor of rat mast cells. Biochem J 1980, 188:789-798.
78. 7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 2003, 23:1320-1328.
79. 7) receptors regulate intracellular calcium and purine release. Neuroreport 1996, 7:2533-2537.
80. 2+ signaling. J Neurosci 2006, 26:1378-1385.
81. Kucher B.M., Neary J.T. Bi-functional effects of ATP/P2 receptor activation on tumor necrosis factor-α release in lipopolysaccharide-stimulated astrocytes. J Neurochem 2005, 92:525-535.
82. Walter L., Dinh T., Stella N. ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. J Neurosci 2004, 24:8068-8074.
83. 7 receptors in rat cultured neocortical astroglia. Br J Pharmacol 2010, 160:1941-1952.
84. 7 receptors in Muller glial cells from the human retina. J Neurosci 2000, 20:5965-5972.
85. Oliveira JF, Riedel T, Leichsenring A, Heine C, Franke H, Krügel U, et al. Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb Cortex 2010; Sep 14. [Epub ahead of print].
86. Nakazawa K. ATP-activated current and its interaction with acetylcholine-activated current in rat sympathetic neurons. J Neurosci 1994, 14:740-750.
87. Khakh B.S., Zhou X., Sydes J., Galligan J.J., Lester H.A. State-dependent cross-inhibition between transmitter-gated cation channels. Nature 2000, 406:405-410.
88. 2 receptor channels. J Biol Chem 2004, 279:52517-52525.
89. A and cationic P2X ionotropic receptors of rat dorsal root ganglion neurons. J Neurosci 2001, 21:4958-4968.
90. Pankratov Y.V., Lalo U.V., Krishtal O.A. Role for P2X receptors in long-term potentiation. J Neurosci 2002, 22:8363-8369.
91. Rycroft B.K., Gibb A.J. Inhibitory interactions of calcineurin (phosphatase 2B) and calmodulin on rat hippocampal NMDA receptors. Neuropharmacology 2004, 47:505-514.
92. Rycroft B.K., Gibb A.J. Regulation of single NMDA receptor channel activity by alpha-actinin and calmodulin in rat hippocampal granule cells. J Physiol, Lond 2004, 557:795-808.
93. Gordon G.R., Baimoukhametova D.V., Hewitt S.A., Rajapaksha W.R., Fisher T.E., Bains J.S. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 2005, 8:1078-1086.
94. Jarvis M.F., Khakh B.S. ATP-gated P2X cation-channels. Neuropharmacology 2009, 56:208-215.
95. 1 receptor membrane redistribution and down-regulation visualized by using receptor-coupled green fluorescent protein chimeras. Neuropharmacology 2000, 39:2054-2066.
96. Bobanovic L.K., Royle S.J., Murrell-Lagnado R.D. P2X receptor trafficking in neurons is subunit specific. J Neurosci 2002, 22:4814-4824.
97. 1 receptor mobility and trafficking; regulation by receptor insertion and activation. J Neurochem 2010, 113:1177-1187.
98. Murrell-Lagnado R.D., Qureshi O.S. Assembly and trafficking of P2X purinergic receptors. Mol Membr Biol 2008, 25:321-331. [Review].
99. Agulhon C., Petravicz J., McMullen A.B., Sweger E.J., Minton S.K., Taves S.R., et al. What is the role of astrocyte calcium in neurophysiology?. Neuron 2008, 59:932-946.
100. 2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 2006, 9:816-823.
101. Kirischuk S., Moller T., Voitenko N., Kettenmann H., Verkhratsky A. ATP-induced cytoplasmic calcium mobilization in Bergmann glial cells. J Neurosci 1995, 15:7861-7871.
102. 3-sensitive internal stores in mammalian oligodendrocytes. J Physiol, Lond 1995, 483:41-57.
103. Verkhratsky A., Orkand R.K., Kettenmann H. Glial calcium: homeostasis and signaling function. Physiol Rev 1998, 78:99-141.
104. Fields R.D., Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 2006, 7:423-436.
105. 2+ signaling in Bergmann glial cells in situ. FASEB J 1997, 11:566-572.
106. Deitmer J.W., Rose C.R. Ion changes and signalling in perisynaptic glia. Brain Res Rev 2010, 63:113-129.
107. Kirischuk S., Kettenmann H., Verkhratsky A. Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch 2007, 454:245-252.
108. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403:316-321.
109. Wu Y., Wang W., Diez-Sampedro A., Richerson G.B. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 2007, 56:851-865.
110. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J Exp Biol 2006, 209:2304-2311.
111. 7 and the inflammasome. Trends Pharmacol Sci 2007, 28:465-472.
112. Franke H., Grosche J., Schadlich H., Krugel U., Allgaier C., Illes P. P2X receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 2001, 108:421-429.
113. 7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 2004, 63:686-699.
114. Egan T.M., Samways D.S., Li Z. Biophysics of P2X receptors. Pflugers Arch 2006, 452:501-512.