Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2011 (2011), Article ID 537659, 12 pages
http://dx.doi.org/10.1155/2011/537659
Research Article

Diacylglycerol Signaling Underlies Astrocytic ATP Release

1Department of Neuroscience, Tufts University, 136 Harrison Avenue, Boston, MA 02111, USA
2Department of Neuroscience, Perelman School of Medicine at University of Pennsylvania, Philadelphia, PA 19104, USA

Received 7 January 2011; Accepted 5 May 2011

Academic Editor: Stuart C. Mangel

Copyright © 2011 Alison E. Mungenast. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. O. Pascual, K. B. Casper, C. Kubera et al., “Astrocytic purinergic signaling coordinates synaptic networks,” Science, vol. 310, no. 5745, pp. 113–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Montana, E. B. Malarkey, C. Verderio, M. Matteoli, and V. Parpura, “Vesicular transmitter release from astrocytes,” Glia, vol. 54, no. 7, pp. 700–715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Agulhon, T. A. Fiacco, and K. D. McCarthy, “Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling,” Science, vol. 327, no. 5970, pp. 1250–1254, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. N. Kang, J. Xu, Q. Xu, M. Nedergaard, and J. Kang, “Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons,” Journal of Neurophysiology, vol. 94, no. 6, pp. 4121–4130, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. V. Montana, Y. Ni, V. Sunjara, X. Hua, and V. Parpura, “Vesicular glutamate transporter-dependent glutamate release from astrocytes,” Journal of Neuroscience, vol. 24, no. 11, pp. 2633–2642, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Bezzi, V. Gundersen, J. L. Galbete et al., “Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate,” Nature Neuroscience, vol. 7, no. 6, pp. 613–620, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. Q. Zhang, T. Pangršič, M. Kreft et al., “Fusion-related release of glutamate from astrocytes,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 12724–12733, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. Q. Zhang, M. Fukuda, E. Van Bockstaele, O. Pascual, and P. G. Haydon, “Synaptotagmin IV regulates glial glutamate release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 25, pp. 9441–9446, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Henneberger, T. Papouin, S. H. R. Oliet, and D. A. Rusakov, “Long-term potentiation depends on release of d-serine from astrocytes,” Nature, vol. 463, no. 7278, pp. 232–236, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. Z. Zhuang, B. Yang, M. H. Theus et al., “EphrinBs regulate D-serine synthesis and release in astrocytes,” Journal of Neuroscience, vol. 30, no. 47, pp. 16015–16024, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. E. A. Newman, “Glial cell inhibition of neurons by release of ATP,” Journal of Neuroscience, vol. 23, no. 5, pp. 1659–1666, 2003. View at Google Scholar · View at Scopus
  12. J. M. Zhang, H. Wang, C. Q. Ye et al., “ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression,” Neuron, vol. 40, no. 5, pp. 971–982, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. G. R. J. Gordon, D. V. Baimoukhametova, S. A. Hewitt, W. R. A. Rajapaksha, T. E. Fisher, and J. S. Bains, “Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy,” Nature Neuroscience, vol. 8, no. 8, pp. 1078–1086, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. M. P. Abbracchio, G. Burnstock, A. Verkhratsky, and H. Zimmermann, “Purinergic signalling in the nervous system: an overview,” Trends in Neurosciences, vol. 32, no. 1, pp. 19–29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. Z. Cai, G. P. Schools, and H. K. Kimelberg, “Metabotropic glutamate receptors in acutely isolated hippocampal astrocytes: developmental changes of mGluR5 mRNA and functional expression,” Glia, vol. 29, no. 1, pp. 70–80, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. A. N. van den Pol, C. Romano, and P. Ghosh, “Metabotropic glutamate receptor mGluR5 subcellular distribution and developmental expression in hypothalamus,” Journal of Comparative Neurology, vol. 362, no. 1, pp. 134–150, 1995. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Fellin, O. Pascual, S. Gobbo, T. Pozzan, P. G. Haydon, and G. Carmignoto, “Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors,” Neuron, vol. 43, no. 5, pp. 729–743, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. M. D'Ascenzo, T. Fellin, M. Terunuma et al., “mGluR5 stimulates gliotransmission in the nucleus accumbens,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 6, pp. 1995–2000, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Hisatsune, K. Nakamura, Y. Kuroda, T. Nakamura, and K. Mikoshiba, “Amplification of Ca2+ signaling by diacylglycerol-mediated inositol 1,4,5-trisphosphate production,” Journal of Biological Chemistry, vol. 280, no. 12, pp. 11723–11730, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. T. V. Dunwiddie and L. Diao, “Extracellular adenosine concentrations in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses,” Journal of Pharmacology and Experimental Therapeutics, vol. 268, no. 2, pp. 537–545, 1994. View at Google Scholar · View at Scopus
  21. S. A. Masino, L. Diao, P. Illes et al., “Modulation of hippocampal glutamatergic transmission by ATP is dependent on adenosine A1 receptors,” Journal of Pharmacology and Experimental Therapeutics, vol. 303, no. 1, pp. 356–363, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. G. F. Tian, H. Azmi, T. Takano et al., “An astrocytic basis of epilepsy,” Nature Medicine, vol. 11, no. 9, pp. 973–981, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. T. V. Dunwiddie and S. A. Masino, “The role and regulation of adenosine in the central nervous system,” Annual Review of Neuroscience, vol. 24, pp. 31–55, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Boison, “Adenosine and epilepsy: from therapeutic rationale to new therapeutic strategies,” The Neuroscientist, vol. 11, no. 1, pp. 25–36, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Mérida, A. Avila-Flores, and E. Merino, “Diacylglycerol kinases: at the hub of cell signalling,” Biochemical Journal, vol. 409, no. 1, pp. 1–18, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. S. M. Prescott and P. W. Majerus, “Characterization of 1,2-diacylglycerol hydrolysis in human platelets. Demonstration of an arachidonoyl-monoacylglycerol intermediate,” Journal of Biological Chemistry, vol. 258, no. 2, pp. 764–769, 1983. View at Google Scholar · View at Scopus
  27. B. D. Boyan, V. L. Sylvia, D. D. Dean, and Z. Schwartz, “Membrane mediated signaling mechanisms are used differentially by metabolites of vitamin D3 in musculoskeletal cells,” Steroids, vol. 67, no. 6, pp. 421–427, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. K. M. Turner, R. D. Burgoyne, and A. Morgan, “Protein phosphorylation and the regulation of synaptic membrane traffic,” Trends in Neurosciences, vol. 22, no. 10, pp. 459–464, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Meggio, A. Donella-Deana, M. Ruzzene et al., “Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2,” The European Journal of Biochemistry, vol. 234, no. 1, pp. 317–322, 1995. View at Google Scholar · View at Scopus
  30. D. Toullec, P. Pianetti, H. Coste et al., “The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C,” Journal of Biological Chemistry, vol. 266, no. 24, pp. 15771–15781, 1991. View at Google Scholar · View at Scopus
  31. R. F. Bruns, F. D. Miller, R. Merriman et al., “Inhibition of protein kinase C by calphostin C is light-dependent,” Biochemical and Biophysical Research Communications, vol. 176, no. 1, pp. 288–293, 1991. View at Google Scholar · View at Scopus
  32. K. D. Wierda, R. F. Toonen, H. de Wit, A. B. Brussaard, and M. Verhage, “Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity,” Neuron, vol. 54, no. 2, pp. 275–290, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. E. B. Malarkey, Y. Ni, and V. Parpura, “Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes,” Glia, vol. 56, no. 8, pp. 821–835, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Chakrabarti and R. Chakrabarti, “Calcium signaling in non-excitable cells: Ca2+ release and influx are independent events linked to two plasma membrane Ca2+ entry channels,” Journal of Cellular Biochemistry, vol. 99, no. 6, pp. 1503–1516, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Zhang, G. Chen, W. Zhou et al., “Regulated ATP release from astrocytes through lysosome exocytosis,” Nature Cell Biology, vol. 9, no. 8, pp. 945–953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Kreft, M. Potokar, M. Stenovec, T. Pangršič, and R. Zorec, “Regulated exocytosis and vesicle trafficking in astrocytes,” Annals of the New York Academy of Sciences, vol. 1152, no. 1, pp. 30–42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. V. Gourine, V. Kasymov, N. Marina et al., “Astrocytes control breathing through pH-dependent release of ATP,” Science, vol. 329, no. 5991, pp. 571–575, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. C. E. Stout, J. L. Costantin, C. C. Naus, and A. Charles, “Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels,” Journal of Biological Chemistry, vol. 277, no. 12, pp. 10482–10488, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Kang, N. Kang, D. Lovatt et al., “Connexin 43 hemichannels are permeable to ATP,” Journal of Neuroscience, vol. 28, no. 18, pp. 4702–4711, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Dröse and K. Altendorf, “Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases,” Journal of Experimental Biology, vol. 200, part 1, pp. 1–8, 1997. View at Google Scholar · View at Scopus
  41. J. S. Davidson, I. M. Baumgarten, and E. H. Harley, “Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid,” Biochemical and Biophysical Research Communications, vol. 134, no. 1, pp. 29–36, 1986. View at Google Scholar · View at Scopus
  42. J. S. Davidson and I. M. Baumgarten, “Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships,” Journal of Pharmacology and Experimental Therapeutics, vol. 246, no. 3, pp. 1104–1107, 1988. View at Google Scholar · View at Scopus
  43. R. Bruzzone, M. T. Barbe, N. J. Jakob, and H. Monyer, “Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes,” Journal of Neurochemistry, vol. 92, no. 5, pp. 1033–1043, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Brose, K. Hofmann, Y. Hata, and T. C. Sudhof, “Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins,” Journal of Biological Chemistry, vol. 270, no. 42, pp. 25273–25280, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. C. S. Bauer, R. Woolley, A. G. Teschemacher, and E. P. Seward, “Potentiation of exocytosis by phospholipase C-coupled G-protein-coupled receptors requires the priming protein Munc13-1,” Journal of Neuroscience, vol. 27, no. 1, pp. 212–219, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Basu, A. Betz, N. Brose, and C. Rosenmund, “Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion,” Journal of Neuroscience, vol. 27, no. 5, pp. 1200–1210, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. S. Andrews-Zwilling, H. Kawabe, K. Reim, F. Varoqueaux, and N. Brose, “Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2,” Journal of Biological Chemistry, vol. 281, no. 28, pp. 19720–19731, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. J. W. Deitmer and A. Araque, “Astrocyte: calcium signaling,” in Encyclopedia of Neuroscience, R. S. Larry, Ed., pp. 565–572, Academic Press, Oxford, UK, 2009. View at Google Scholar
  49. P. B. Guthrie, J. Knappenberger, M. Segal, M. V. L. Bennett, A. Charles, and S. B. Kater, “ATP released from astrocytes mediates glial calcium waves,” Journal of Neuroscience, vol. 19, no. 2, pp. 520–528, 1999. View at Google Scholar · View at Scopus
  50. Y. Ono, T. Fujii, K. Ogita, U. Kikkawa, K. Igarashi, and Y. Nishizuka, “Protein kinase C zeta subspecies from rat brain: its structure, expression and properties,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 9, pp. 3099–3103, 1989. View at Google Scholar · View at Scopus
  51. F. Colon-Gonzalez and M. G. Kazanietz, “C1 domains exposed: from diacylglycerol binding to protein-protein interactions,” Biochimica et Biophysica Acta, vol. 1761, no. 8, pp. 827–837, 2006. View at Google Scholar
  52. H. W. Francis, J. C. Scott, and P. B. Manis, “Protein kinase C mediates potentiation of synaptic transmission by phorbol ester at parallel fibers in the dorsal cochlear nucleus,” Brain Research, vol. 951, no. 1, pp. 9–22, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. R. C. Malenka, D. V. Madison, and R. A. Nicoll, “Potentiation of synaptic transmission in the hippocampus by phorbol esters,” Nature, vol. 321, no. 6066, pp. 175–177, 1986. View at Google Scholar · View at Scopus
  54. R. Shapira, S. D. Silberberg, S. Ginsburg, and R. Rahamimoff, “Activation of protein kinase C augments evoked transmitter release,” Nature, vol. 325, no. 6099, pp. 58–60, 1987. View at Google Scholar · View at Scopus
  55. A. C. Newton, “Regulation of protein kinase C,” Current Opinion in Cell Biology, vol. 9, no. 2, pp. 161–167, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. N. M. Ahmad, V. Rodeschini, N. S. Simpkins, S. E. Ward, and A. J. Blake, “Synthesis of polyprenylated acylphloroglucinols using bridgehead lithiation: the total synthesis of racemic clusianone and a formal synthesis of racemic garsubellin A,” Journal of Organic Chemistry, vol. 72, no. 13, pp. 4803–4815, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. J. S. Rhee, A. Betz, S. Pyott et al., “Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs,” Cell, vol. 108, no. 1, pp. 121–133, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. M. L. Cotrina, J. H. Lin, J. C. López-Garcia, C. C. Naus, and M. Nedergaard, “ATP-mediated glia signaling,” Journal of Neuroscience, vol. 20, no. 8, pp. 2835–2844, 2000. View at Google Scholar · View at Scopus
  59. R. Iglesias, G. Dahl, F. Qiu, D. C. Spray, and E. Scemes, “Pannexin 1: the molecular substrate of astrocyte ‘hemichannels’,” Journal of Neuroscience, vol. 29, no. 21, pp. 7092–7097, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. J. C. Sáez, J. A. Connor, D. C. Spray, and M. V. Bennett, “Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 8, pp. 2708–2712, 1989. View at Google Scholar · View at Scopus
  61. G. S. Goldberg, P. D. Lampe, and B. J. Nicholson, “Selective transfer of endogenous metabolites through gap junctions composed of different connexins,” Nature Cell Biology, vol. 1, no. 7, pp. 457–459, 1999. View at Google Scholar · View at Scopus
  62. A. E. Blum, S. M. Joseph, R. J. Przybylski, and G. R. Dubyak, “Rho-family GTPases modulate Ca2+-dependent ATP release from astrocytes,” The American Journal of Physiology—Cell Physiology, vol. 295, no. 1, pp. C231–C241, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Guan, H. Dai, and J. Rizo, “Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes,” Biochemistry, vol. 47, no. 6, pp. 1474–1481, 2008. View at Publisher · View at Google Scholar · View at Scopus