Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes

Journal of General Physiology

Volumn 129, Issue 6, 2007, Pages 485-491

  Bowser, David N ^a,b   Khakh, Baljit S ^a,c  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; EXTRACELLULAR CALCIUM; EXTRACELLULAR SPACE; GAP JUNCTION; HIPPOCAMPUS; NERVE CELL EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; RAT; SIGNAL TRANSDUCTION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANILINE COMPOUNDS; ANIMALS; APYRASE; ASTROCYTES; BREFELDIN A; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CYTOPLASMIC VESICLES; DIFFUSION; ENZYME INHIBITORS; FLUORESCENT DYES; HIPPOCAMPUS; MACROLIDES; NEURONS; PARACRINE COMMUNICATION; PROTON-TRANSLOCATING ATPASES; PYRIDOXAL PHOSPHATE; RATS; RECEPTORS, PURINERGIC P2; SURAMIN; TIME FACTORS; XANTHENES;

EID: 34249828210     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200709780     Document Type: Article

References (53)

1. Abdelmohsen, K., D. Stuhlmann, F. Daubrawa, and L.-O. Klotz. 2005. Dicumarol is a potent reversible inhibitor of gap junctional intercellular communication. Arch. Biochem. Biophys. 434:241-247.
2. Abdipranoto, A., G.J. Liu, E.L. Werry, and M.R. Bennett. 2003. Mechanisms of secretion of ATP from cortical astrocytes triggered by uridine triphosphate. Neuroreport. 14:2177-2181.
3. Arcuino, G., J.H. Lin, T. Takano, C. Liu, L. Jiang, Q. Gao, J. Kang, and M. Nedergaard. 2002. Intercellular calcium signaling mediated by point-source burst release of ATP. Proc. Natl. Acad. Sci. USA. 99:9840-9845.
4. Bennett, M.R., L. Farnell, and W.G. Gibson. 2005. A quantitative model of purinergic junctional transmission of calcium waves in astrocyte networks. Biophys. J. 89:2235-2250.
5. Bennett, M.R., V. Buljan, L. Farnell, and W.G. Gibson. 2006. Purinergic junctional transmission and propagation of calcium waves in spinal cord astrocyte networks. Biophys. J. 91:3560-3571.
6. Bennett, M.V., J.E. Contreras, F.F. Bukauskas, and J.C. Saez. 2003. New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci. 26:610-617.
7. Bezzi, P., V. Gundersen, J.L. Galbete, G. Seifert, C. Steinhauser, E. Pilati, and A. Volterra. 2004. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci. 7:613-620.
8. Bowser, D.N., and B.S. Khakh. 2004. ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J. Neurosci. 24:8606-8620.
9. Bowser, D.N., and B.S. Khakh. 2007. Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. USA. 104:4212-4217.
10. Buell, G., A.D. Michel, C. Lewis, G. Collo, P.P.A. Humphrey, and A. Surprenant. 1996. P2X1 receptor activation in HL60 cells. Blood. 87:2659-2664.
11. Burnstock, G. 1972. Purinergic nerves. Pharmacol. Rev. 24:509-581.
12. Charles, A. 1998. Intercellular calcium waves in glia. Glia. 24:39-49.
13. Charles, A.C., J.E. Merrill, E.R. Dirksen, and M.J. Sanderson. 1991. Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron. 6:983-992.
14. Chen, X., L. Wang, Y. Zhou, L.H. Zheng, and Z. Zhou. 2005. "Kissand-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J. Neurosci. 25:9236-9243.
15. Coco, S., F. Calegari, E. Pravettoni, D. Pozzi, E. Taverna, P. Rosa, M. Matteoli, and C. Verderio. 2003. Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 278:1354-1362.
16. Cornell-Bell, A.H., S.M. Finkbeiner, M.S. Cooper, and S.J. Smith. 1990. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. 247:470-473.
17. Edwards, F.A., A.J. Gibb, and D. Colquhoun. 1992. ATP receptor-mediated synaptic currents in the central nervous system. Nature. 359:144-147.
18. 2+ wave propagation in dorsal spinal cord astrocytes. J. Neurosci. 20:2800-2808.
19. Fellin, T., O. Pascual, S. Gobbo, T. Pozzan, P.G. Haydon, and G. Carmignoto. 2004. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron. 43:729-743.
20. Fellin, T., J.Y. Sul, M. D'Ascenzo, H. Takano, O. Pascual, and P.G. Haydon. 2006. Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP. Novartis Found Symp. 276:208-217; discussion 217-221, 233-207, 275-281.
21. Fields, R.D., and G. Burnstock. 2006. Purinergic signalling in neuronglia interactions. Nat. Rev. Neurosci. 7:423-436.
22. Fisher, J.A., G. Girdler, and B.S. Khakh. 2004. Time resolved measurement of state specific P2X ion channel cytosolic gating motions. J. Neurosci. 24:10475-10487.
23. Gallagher, C.J., and M.W. Salter. 2003. Differential properties of astrocyte calcium waves mediated by P2Y1 and P2Y2 receptors. J. Neurosci. 23:6728-6739.
24. Granseth, B., B. Odermatt, S.J. Royle, and L. Lagnado. 2006. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron. 51:773-786.
25. Guthrie, P.B., J. Knappenberger, M. Segal, M.V. Bennett, A.C. Charles, and S.B. Kater. 1999. ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19:520-528.
26. Haydon, P.G. 2001. GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2:185-193.
27. Hirase, H., L. Qian, P. Bartho, and G. Buzsaki. 2004. Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 2:E96.
28. Humphrey, P.P., G. Buell, I. Kennedy, B.S. Khakh, A.D. Michel, A. Surprenant, and D.J. Trezise. 1995. New insights on P2X purinoceptors. Naunyn Schmiedebergs Arch. Pharmacol. 352:585-596.
29. Illes, P., and J. Alexandre Ribeiro. 2004. Molecular physiology of P2 receptors in the central nervous system. Eur. J. Pharmacol. 483:5-17.
30. Khakh, B.S. 2001. Molecular physiology of P2X receptors and ATP signalling at synapses. Nat. Rev. Neurosci. 2:165-174.
31. Khakh, B.S., G. Burnstock, C. Kennedy, B.F. King, R.A. North, P. Seguela, M. Voigt, and P.P.A. Humphrey. 2001. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol. Rev. 53:107-118.
32. Koizumi, S., K. Fujishita, M. Tsuda, Y. Shigemoto-Mogami, and K. Inoue. 2003. Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc. Natl. Acad. Sci. USA. 100:11023-11028.
33. Maienschein, V., M. Marxen, W. Volknandt, and H. Zimmermann. 1999. A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia. 26:233-244.
34. Mori, M., C. Heuss, B.H. Gahwiler, and U. Gerber. 2001. Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J. Physiol. 535:115-123.
35. Moro, S., D. Guo, E. Camaioni, J.L. Boyer, T.K. Harden, and K.A. Jacobson. 1998. Human P2Y1 receptor: molecular modeling and site-directed mutagenesis as tools to identify agonist and antagonist recognition sites. J. Med. Chem. 41:1456-1466.
36. Newman, E., and K. Zahs. 1997. Calcium waves in retinal glial cells. Science. 275:844-847.
37. Nieber, K., W. Poelchen, and P. Illes. 1997. Role of ATP in fast excitatory synaptic potentials in locus coeruleus neurones of the rat. Br. J. Pharmacol. 122:423-430.
38. North, R.A. 2002. Molecular physiology of P2X receptors. Physiol. Rev. 82:1013-1067.
39. Pankratov, Y., E. Castro, M.T. Miras-Portugal, and O. Krishtal. 1998. A purinergic component of the excitatory postsynaptic current mediated by P2X receptors in the CA1 neurons of the rat hippocampus. Eur. J. Neurosci. 10:3898-3902.
40. Pankratov, Y., U. Lalo, A. Verkhratsky, and R.A. North. 2007. Quantal release of ATP in mouse cortex. J. Gen. Physiol. 129:257-265.
41. Pankratov, Y.V., U.V. Lalo, and O.A. Krishtal. 2002. Role for P2X receptors in long-term potentiation. J. Neurosci. 22:8363-8369.
42. Pasti, L., M. Zonta, T. Pozzan, S. Vicini, and G. Carmignoto. 2001. Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J. Neurosci. 21:477-484.
43. Porter, J.T., and K.D. McCarthy. 1996. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16:5073-5081.
44. Queiroz, G., D.K. Meyer, A. Meyer, K. Starke, and I. von Kugelgen. 1999. A study of the mechanism of the release of ATP from rat cortical astroglial cells evoked by activation of glutamate receptors. Neuroscience. 91:1171-1181.
45. Scemes, E., and C. Giaume. 2006. Astrocyte calcium waves: what they are and what they do. Glia. 54:716-725.
46. Scemes, E., S.O. Suadicani, and D.C. Spray. 2000. Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J. Neurosci. 20:1435-1445.
47. Suadicani, S.O., C.E. Flores, M. Urban-Maldonado, M. Beelitz, and E. Scemes. 2004. Gap junction channels coordinate the propagation of intercellular Ca2+ signals generated by P2Y receptor activation. Glia. 48:217-229.
48. 2+ signaling. J. Neurosci. 26:1378-1385.
49. Tian, G.F., H. Azmi, T. Takano, Q. Xu, W. Peng, J. Lin, N. Oberheim, N. Lou, X. Wang, H.R. Zielke, et al. 2005. An astrocytic basis of epilepsy. Nat. Med. 11:973-981.
50. Tian, G.F., T. Takano, J.H. Lin, X. Wang, L. Bekar, and M. Nedergaard. 2006. Imaging of cortical astrocytes using 2-photon laser scanning microscopy in the intact mouse brain. Adv. Drug Deliv. Rev. 58:773-787.
51. 2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9:816-823.
52. Wirkner, K., A. Gunther, M. Weber, S.J. Guzman, T. Krause, J. Fuchs, L. Koles, W. Norenberg, and P. Illes. 2007. Modulation of NMDA receptor current in layer V pyramidal neurons of the rat prefrontal cortex by P2Y receptor activation. Cereb. Cortex. 17:621-631.
53. Zhang, Q., T. Pangrsic, M. Kreft, M. Krzan, N. Li, J.Y. Sul, M. Halassa, E. Van Bockstaele, R. Zorec, and P.G. Haydon. 2004. Fusion-related release of glutamate from astrocytes. J. Biol. Chem. 279:12724-12733.