P2Y1 receptor inhibits GABA transport through a calcium signalling-dependent mechanism in rat cortical astrocytes

GLIA

Volumn 62, Issue 8, 2014, Pages 1211-1226

  Jacob, Pedro F ^a,b   Vaz, Sandra H ^a,b   Ribeiro, Joaquim A ^a,b   Sebastião, Ana M ^a,b  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Astrocytes; ATP; Calcium signalling; GABA transporters

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; 4 AMINOBUTYRIC ACID; ADENOSINE; ADENOSINE DEAMINASE; ADENOSINE TRIPHOSPHATE; CALCIUM; CYCLOPIAZONIC ACID; GABA TRANSPORTER 1; GABA TRANSPORTER 3; PURINERGIC P2Y RECEPTOR ANTAGONIST; PURINERGIC P2Y1 RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PROTEIN KINASE C; SLC6A11 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM DEPLETION; CALCIUM SIGNALING; CHELATION; CONTROLLED STUDY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; ACTIVE TRANSPORT; ANIMAL; BRAIN CORTEX; CELL CULTURE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT, ACTIVE; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CEREBRAL CORTEX; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; PHOSPHOINOSITIDE PHOSPHOLIPASE C; PROTEIN KINASE C; RATS, WISTAR; RECEPTORS, PURINERGIC P2Y1;

EID: 84902320430     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22673     Document Type: Article

References (79)

1. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. 2006. International union of pharmacology LVIII: Update on the P2Y G protein-coupled nucleotide receptors: From molecular mechanisms and pathophysiology. Pharmacol Rev 58:281-341.
2. 2+ dynamics in synaptosomes isolated from the squid optic lobe. J Neurosci Res 62:840-846.
3. Bers DM, Ginsburg KS. 2007. Na:Ca stoichiometry and cytosolic Ca-dependent activation of NCX in intact cardiomyocytes. Ann N Y Acad Sci 1099:326-338.
4. Biedermann B, Bringmann A, Reichenbach A. 2002. High-affinity GABA uptake in retinal glial (Müller) cells of the guinea pig: Electrophysiological characterization, immunohistochemical localization, and modeling of efficiency. Glia 39:217-228.
5. Borden LA. 1996. GABA transporter heterogeneity: Pharmacology and cellular localization. Neurochem Int 29:335-356.
6. Boyer JL, Mohanram A, Camaioni E, Jacobson KA, Harden TK. 1998. Competitive and selective antagonism of P2Y1 receptors by N6-methyl 2′-deoxyadenosine 3′, 5′-bisphosphate. Br J Pharmacol 124:1-3.
7. Bronstein J, Nishimura R, Lasher R, Cole R, de Vellis J, Farber D, Wasterlain C. 1988. Calmodulin kinase II in pure cultured astrocytes. J Neurochem 50:45-49.
8. Brown SG, King BF, Kim YC, Jang SY, Burnstock G, Jacobson KA. 2000. Activity of novel adenine nucleotide derivatives as agonists and antagonists at recombinant rat P2X receptors. Drug Dev Res 49:253-259.
9. Bruner G, Murphy S. 1990. ATP-evoked arachidonic acid mobilization in astrocytes is via a P2Y-purinergic receptor. J Neurochem 55:1569-1575.
10. Burnstock G. 2008. Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7:575-590.
11. Burnstock G, Krügel U, Abbracchio MP, Illes P. 2011. Purinergic signalling: From normal behaviour to pathological brain function. Prog Neurobiol 95:229-274.
12. 2+ responses evoked by ATP and other nucleotides in mammalian brain astrocytes. Br J Pharmacol 121:1700-1706.
13. 2+ pump inhibitor. Am J Physiol Cell Physiol 280:C1027-C1030.
14. Chéramy A, Artaud F, Godeheu G, L'hirondel M, Glowinski J. 1996. Stimulatory effect of arachidonic acid on the release of GABA in matrix-enriched areas from the rat striatum. Brain Res 742:185-194.
15. Conti F, Minelli A, Melone M. 2004. GABA transporters in the mammalian cerebral cortex: Localization, development and pathological implications. Brain Res Brain Res Rev 45:196-212.
16. Corey JL, Davidson N, Lester HA, Brecha N, Quick MW. 1994. Protein kinase C modulates the activity of a cloned gamma-aminobutyric acid transporter expressed in Xenopus oocytes via regulated subcellular redistribution of the transporter. J Biol Chem 269:14759-14767.
17. Cristóvão-Ferreira S, Navarro G, Brugarolas M, Pérez-Capote K, Vaz SH, Fattorini G, Conti F, Lluis C, Ribeiro JA, McCormick PJ, Casadó V, Franco R, Sebastião AM. 2013. A1R-A2AR heteromers coupled to Gs and G i/0 proteins modulate GABA transport into astrocytes. Purinergic Signal 9:433-449.
18. Cristóvão-Ferreira S, Vaz SH, Ribeiro JA, Sebastião AM. 2009. Adenosine A2A receptors enhance GABA transport into nerve terminals by restraining PKC inhibition of GAT-1. J Neurochem 109:336-347.
19. Cunha RA, Ribeiro JA. 1999. Facilitation of GABA release by arachidonic acid in rat hippocampal synaptosomes. Eur J Neurosci 11:2171-2174.
20. Cupello A, Mainardi P, Robello M, Thellung S. 1997. Effect of nitric oxide donors on GABA uptake by rat brain synaptosomes. Neurochem Res 22:1517-1521.
21. Duarte CB, Santos PF, Sánchez-Prieto J, Carvalho AP. 1996. Glutamate release evoked by glutamate receptor agonists in cultured chick retina cells: Modulation by arachidonic acid. J Neurosci Res 44:363-373.
22. Erb L, Liao Z, Seye CI, Weisman GA. 2006. P2 receptors: Intracellular signaling. Pflugers Arch 452:552-562.
23. 2+ wave propagation in dorsal spinal cord astrocytes. J Neurosci 20:2800-2808.
24. Fan HP, Fan FJ, Bao L, Pei G. 2006. SNAP-25/syntaxin 1A complex functionally modulates neurotransmitter gamma-aminobutyric acid reuptake. J Biol Chem 281:28174-28184.
25. 2+ by P2X and P2Y receptor-subtypes in cultured cortical astroglia of the rat. Neuroscience 160:767-783.
26. Fresu L, Dehpour A, Genazzani AA, Carafoli E, Guerini D. 1999. Plasma membrane calcium ATPase isoforms in astrocytes. Glia 28:150-155.
27. Fumagalli M, Brambilla R, D'Ambrosi N, Volonté C, Matteoli M, Verderio C, Abbracchio MP. 2003. Nucleotide-mediated calcium signaling in rat cortical astrocytes: Role of P2X and P2Y receptors. Glia 43:218-230.
28. 13 receptor. Biochem Pharmacol 68:113-124.
29. 2+ and calmodulin-dependent enzymes in the regulation of glycine transport in Müller glia. J Neurochem 80:634-645.
30. 2+ stores in astrocytes. Glia 31:15-28.
31. Gomeza J, Casado M, Gimenez C, Aragon C. 1991. Inhibition of high-affinity gamma-aminobutyric acid uptake in primary astrocyte cultures by phorbol esters and phospholipase C. Biochem J 275:435-439.
32. 2+ in isolated synaptic plasma membrane vesicles. Brain Res Mol Brain Res 51:106-114.
33. Graupner M, Erler F, Meyer-Hermann M. 2005. A theory of plasma membrane calcium pump stimulation and activity. J Biol Phys 31:183-206.
34. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
35. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB. 1999. ATP released from astrocytes mediates glial calcium waves. J Neurosci 19:520-528.
36. Halassa MM, Fellin T, Haydon PG. 2007. The tripartite synapse: Roles for gliotransmission in health and disease. Trends Mol Med 13:54-63.
37. Hamby ME, Uliasz TF, Hewett SJ, Hewett JA. 2006. Characterization of an improved procedure for the removal of microglia from confluent monolayers of primary astrocytes. J Neurosci Methods 150:128-137.
38. + depolarization evokes ATP, adenosine and glutamate release from glia in rat hippocampus: A microelectrode biosensor study. Br J Pharmacol 167:1003-1020.
39. Héja L, Barabás P, Nyitrai G, Kékesi KA, Lasztóczi B, Toke O, Tárkányi G, Madsen K, Schousboe A, Dobolyi A, Palkovits M, Kardos J. 2009. Glutamate uptake triggers transporter-mediated GABA release from astrocytes. PLoS One 4:e7153.
40. 2+ exchanger. J Biol Chem 287:31641-31649.
41. Hollopeter G, Jantzen HM, Vincent D, Li G, England L, Ramakrishnan V, Yang RB, Nurden P, Nurden A, Julius D, Conley PB. 2001. Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 409:202-207.
42. Hu J, Quick MW. 2008. Substrate-mediated regulation of gamma-aminobutyric acid transporter 1 in rat brain. Neuropharmacology 54:309-318.
43. 2+ exchange in cells expressing NCX1. J Biol Chem 271:22391-22397.
44. 2+ exchanger in vascular smooth muscle, and in neurons and astrocytes. Ann N Y Acad Sci 779:318-335.
45. Kanner BI. 2006. Structure and function of sodium-coupled GABA and glutamate transporters. J Membr Biol 213:89-100.
46. Kim WT, Rioult MG, Cornell-Bell AH. 1994. Glutamate-induced calcium signaling in astrocytes. Glia 11:173-184.
47. Kirischuk S, Parpura V, Verkhratsky A. 2012. Sodium dynamics: Another key to astroglial excitability? Trends Neurosci 35:497-506.
48. 1 receptor-mediated nitric oxide production. Neuropsychopharmacology 28:435-444.
49. Kristensen AS, Andersen J, Jørgensen TN, Sørensen L, Eriksen J, Loland CJ, Strømgaard K, Gether U. 2011. SLC6 neurotransmitter transporters: Structure, function, and regulation. Pharmacol Rev 63:585-640.
50. Kumaria A, Tolias CM, Burnstock G. 2008. ATP signalling in epilepsy. Purinergic Signal 4:339-346.
51. Liu GX, Cai GQ, Cai YQ, Sheng ZJ, Jiang J, Mei Z, Wang ZG, Guo L, Fei J. 2007. Reduced anxiety and depression-like behaviors in mice lacking GABA transporter subtype 1. Neuropsychopharmacology 32:1531-1539.
52. Llinás R, McGuinness TL, Leonard CS, Sugimori M, Greengard P. 1985. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc Natl Acad Sci USA 82:3035-3039.
53. Mager S, Naeve J, Quick M, Labarca C, Davidson N, Lester HA. 1993. Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron 10:177-188.
54. Marteau F, Le Poul E, Communi D, Communi D, Labouret C, Savi P, Boeynaems JM, Gonzalez NS. 2003. Pharmacological characterization of the human P2Y13 receptor. Mol Pharmacol 64:104-112.
55. McCarthy KD, de Vellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
56. Minelli A, Brecha NC, Karschin C, DeBiasi S, Conti F. 1995. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J Neurosci 15:7734-7746.
57. Minelli A, DeBiasi S, Brecha NC, Zuccarello LV, Conti F. 1996. GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex. J Neurosci 16:6255-6264.
58. Nicholas RA. 2001. Identification of the P2Y(12) receptor: A novel member of the P2Y family of receptors activated by extracellular nucleotides. Mol Pharmacol 60:416-420.
59. Nishio H, Nezasa K, Nakata Y. 1995. Role of calcium ion in platelet serotonin uptake regulation. Eur J Pharmacol 288:149-155.
60. Parpura V, Liu F, Jeftinija KV, Haydon PG, Jeftinija SD. 1995. Neuroligand-evoked calcium-dependent release of excitatory amino acids from Schwann cells. J Neurosci 15:5831-5839.
61. + signalling. Transl Neurosci 3:334-344.
62. Perea G, Navarrete M, Araque A. 2009. Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci 32:421-431.
63. Radian R, Kanner BI. 1983. Stoichiometry of sodium- and chloride-coupled gamma-aminobutyric acid transport by synaptic plasma membrane vesicles isolated from rat brain. Biochemistry 22:1236-1241.
64. 2+ exchangers. Br J Pharmacol 165:922-936.
65. Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, Konnerth A. 2003. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 426:74-78.
66. Saura J. 2007. Microglial cells in astroglial cultures: A cautionary note. J Neuroinflammation 4:1-11.
67. Schmitt U, Lüddens H, Hiemke C. 2002. Anxiolytic-like effects of acute and chronic GABA transporter inhibition in rats. J Neural Transm 109:871-880.
68. 12 nucleotide receptor of brain capillary endothelial cells. J Biol Chem 277:31390-31400.
69. Shigetomi E, Bowser DN, Sofroniew MV, Khakh BS. 2008. Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J Neurosci 28:6659-6653.
70. Sitges M, Dunkley PR, Chiu LM. 1995. A role for calcium/calmodulin kinase(s) in the regulation of GABA exocytosis. Neurochem Res 20:245-252.
71. Toullec D, Pianetti P, Coste H, Belleverque P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F, Duhamel L, Charon D, Kirilovsky J. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266:15771-15781.
72. Vaz SH, Jørgensen TN, Cristóvão-Ferreira S, Duflot S, Ribeiro JA, Gether U, Sebastião AM. 2011. Brain-derived neurotrophic factor (BDNF) enhances GABA transport by modulating the trafficking of GABA transporter-1 (GAT-1) from the plasma membrane of rat cortical astrocytes. J Biol Chem 286:40464-40476.
73. von Kügelgen I. 2006. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol Ther 110:415-432.
74. Waldo GL, Harden TK. 2004. Agonist binding and Gq-stimulating activities of the purified human P2Y1 receptor. Mol Pharmacol 65:426-436.
75. 2+ exchange current in guinea-pig cardiac ventricular cells. Br J Pharmacol 119:555-563.
76. Weng J-Y, Hsu T-T, Sun SH. 2008. Functional characterization of P2Y1 versus P2X receptors in RBA-2 astrocytes: Elucidate the roles of ATP release and protein kinase C. J Cell Biochem 104:554-567.
77. Wu Y, Wang W, Díez-Sampedro A, Richerson GB. 2007. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851-865.
78. Wu Y, Wang W, Richerson GB. 2003. Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J Neurophysiol 65:426-436.
79. Zimmermann H, Zebisch M, Sträter N. 2012. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8:437-502.