P2Y receptor mediated inhibitory modulation of noradrenaline release in response to electrical field stimulation and ischemic conditions in superfused rat hippocampus slices

Journal of Neurochemistry

Volumn 106, Issue 1, 2008, Pages 347-360

  Csölle, Cecília ^a   Heinrich, Attila ^a   Kittel, Ágnes ^a   Sperlágh, Beáta ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Hippocampus; Ischemia; Noradrenaline; P2X receptor; P2Y receptor; Release

Indexed keywords

2 AMINO 4 PHOSPHONOBUTYRIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; BICUCULLINE; CALCIUM; GLUCOSE; MESSENGER RNA; NORADRENALIN; OXYGEN; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2Y RECEPTOR; TRITIUM;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BRAIN PERFUSION; BRAIN SLICE; BRAIN STEM; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; ELECTRIC FIELD; ELECTROSTIMULATION; ENZYME INHIBITION; ENZYME LOCALIZATION; GRANULE CELL; HIPPOCAMPUS; IMMUNOREACTIVITY; INTERNEURON; ISCHEMIA; MOSSY FIBER; NEUROTRANSMITTER RELEASE; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; RAT;

ANIMALS; DENDRITES; DENTATE GYRUS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; MALE; MOSSY FIBERS, HIPPOCAMPAL; NEURAL INHIBITION; NOREPINEPHRINE; ORGAN CULTURE TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

RATTUS;

EID: 45249121235     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05391.x     Document Type: Article

References (65)

1. Abbracchio M. P., Burnstock G., Boeynaems J. M. 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.
2. 2+-independent release of neurotransmitters. J. Neurochem. 58, 395 405.
3. Barik J. Wonnacott S. (2006) Indirect modulation by alpha7 nicotinic acetylcholine receptors of noradrenaline release in rat hippocampal slices: interaction with glutamate and GABA systems and effect of nicotine withdrawal. Mol. Pharmacol. 69, 618 628.
4. Boehm S. (1999) ATP stimulates sympathetic transmitter release via presynaptic P2X purinoceptors. J. Neurosci. 19, 737 746.
5. Boehm S. Kubista H. (2002) Fine tuning of sympathetic transmitter release via ionotropic and metabotropic presynaptic receptors. Pharmacol. Rev. 54, 43 99.
6. Borst M. M. Schrader J. (1991) Adenine nucleotide release from isolated perfused guinea pig hearts and extracellular formation of adenosine. Circ. Res. 68, 797 806.
7. Bowser D. N. Khakh B. S. (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J. Neurosci. 24, 8606 8620.
8. Buller K. M., Khanna S., Sibbald J. R. Day T. A. (1996) Central noradrenergic neurons signal via ATP to elicit vasopressin responses to haemorrhage. Neuroscience 73, 637 642.
9. Burnstock G. (2006) Purinergic signalling - an overview. Novartis Found. Symp. 276, 26 48 Discussion 48 57, 275 281.
10. Cadet J. L. Brannock C. (1998) Free radicals and the pathobiology of brain dopamine systems. Neurochem. Int. 32, 117 131.
11. Chhatriwala M., Ravi R. G., Patel R. I., Boyer J. L., Jacobson K. A. Harden T. K. (2004) Induction of novel agonist selectivity for the ADP-activated P2Y1 receptor versus the ADP-activated P2Y12 and P2Y13 receptors by conformational constraint of an ADP analog. J. Pharmacol. Exp. Ther. 311, 1038 1043.
12. Cunha R. A. Ribeiro J. A. (2000) ATP as a presynaptic modulator. Life Sci. 68, 119 137.
13. Cunha R. A., Vizi E. S., Ribeiro J. A. Sebastiao A. M. (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.
14. Cunha R. A., Sebastiao A. M. Ribeiro J. A. (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.
15. Erecinska M. Silver I. A. (1996) Calcium handling by hippocampal neurons under physiologic and pathologic conditions. Adv. Neurol. 71, 119 136.
16. Fassio A., Rossi F., Bonanno G. Raiteri M. (1999) GABA induces norepinephrine exocytosis from hippocampal noradrenergic axon terminals by a dual mechanism involving different voltage-sensitive calcium channels. J. Neurosci. Res. 57, 324 331.
17. + channels in neurons. Br. J. Pharmacol. 129, U30 U30.
18. Frenguelli B. G., Wigmore G., Llaudet E. Dale N. (2007) Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus. J. Neurochem. 101, 1400 1413.
19. Frohlich R., Boehm S. Illes P. (1996) Pharmacological characterization of P2 purinoceptor types in rat locus coeruleus neurons. Eur. J. Pharmacol. 315, 255 261.
20. Fumagalli M., Trincavelli L., Lecca D., Martini C., Ciana P. Abbracchio M. P. (2004) Cloning, pharmacological characterisation and distribution of the rat G-protein-coupled P2Y(13) receptor. Biochem. Pharmacol. 68, 113 124.
21. Guo C., Masin M., Qureshi O. S. Murrell-Lagnado R. D. (2007) Evidence for functional P2X4/P2X7 heteromeric receptors. Mol. Pharmacol. 72, 1447 1456.
22. Hollopeter G., Jantzen H. M., Vincent D. et al. (2001) Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 409, 202 207.
23. Hussl S. Boehm S. (2006) Functions of neuronal P2Y receptors. Pflugers Arch. 452, 538 551.
24. Inoue K. (1998) ATP receptors for the protection of hippocampal functions. Jpn. J. Pharmacol. 78, 405 410.
25. Jacobson K. A., Costanzi S., Joshi B. V., Besada P., Shin D. H., Ko H., Ivanov A. A. Mamedova L. (2006) Agonists and antagonists for P2 receptors. Novartis Found. Symp. 276, 58 68 Discussion 68 72, 107 112, 275 181.
26. Jonzon B. Fredholm B. B. (1984) Adenosine receptor mediated inhibition of noradrenaline release from slices of the rat hippocampus. Life Sci. 35, 1971 1979.
27. 3H]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices. Brain Res. 823, 183 190.
28. 2+concentration in isolated nerve terminals following metabolic inhibition: possible relevance to hypoglycaemia and anoxia. Neuroscience 27, 175 182.
29. Kawamura M., Gachet C., Inoue K. Kato F. (2004) Direct excitation of inhibitory interneurons by extracellular ATP mediated by P2Y1 receptors in the hippocampal slice. J. Neurosci. 24, 10835 10845.
30. Khakh B. S., Gittermann D., Cockayne D. A. Jones A. (2003) ATP modulation of excitatory synapses onto interneurons. J. Neurosci. 23, 7426 7437.
31. 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.
32. von Kugelgen I. (2006) Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110, 415 432.
33. 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.
34. Luthardt J., Borvendeg J. S., Sperlágh B. Illes P. (2002) P2Y receptor activation inhibits NMDA receptor-channels in layer V pyramidal neurons of the rat prefrontal and parietal cortex. Neurochem. Int. 1238, 1 12.
35. Melani A., Turchi D., Vannucchi M. G., Cipriani S., Gianfriddo M. Pedata F. (2005) ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem. Int. 47, 442 448.
36. Milusheva E. A. Baranyi M. (2003) Implication of ionotropic glutamate receptors in the release of noradrenaline in hippocampal CA1 and CA3 subregions under oxygen and glucose deprivation. Neurochem. Int. 43, 543 550.
37. Milusheva E., Doda M., Pasztor E., Lajtha A., Sershen H. Vizi E. S. (1992) Regulatory interactions among axon terminals affecting the release of different transmitters from rat striatal slices under hypoxic and hypoglycemic conditions. J. Neurochem. 59, 946 952.
38. 3H]noradrenaline in response to oxidative stress combined with mitochondrial dysfunction in rat hippocampal slices. Neuroscience 120, 771 781.
39. Moran-Jimenez M. J. Matute C. (2000) Immunohistochemical localization of the P2Y(1) purinergic receptor in neurons and glial cells of the central nervous system. Brain Res. 78, 50 58.
40. Mori M., Heuss C., Gahwiler B. H. Gerber U. (2001) Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J. Physiol. 535, 115 123.
41. 3H]noradrenaline and glutamate in response to simulation of ischemic conditions in rat spinal cord slice preparation: effect of NMDA and AMPA receptor antagonists. Eur. J. Pharmacol. 366, 143 150.
42. Oleskevich S., Descarries L. Lacaille J. C. (1989) Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J. Neurosci. 9, 3803 3815.
43. Pankratov Y., Castro E., Miras-Portugal M. T. Krishtal O. (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.
44. Pankratov Y. V., Lalo U. V. Krishtal O. A. (2002) Role for P2X receptors in long-term potentiation. J. Neurosci. 22, 8363 8369.
45. Papp L., Balazsa T., Kofalvi A., Erdelyi F., Szabo G., Vizi E. S. Sperlagh B. (2004) P2X receptor activation elicits transporter-mediated noradrenaline release from rat hippocampal slices. J. Pharmacol. Exp. Ther. 310, 973 980.
46. Pittaluga A. Raiteri M. (1992) N-methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. I. Location on axon terminals and pharmacological characterization. J. Pharmacol. Exp. Ther. 260, 232 237.
47. 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.
48. Ralevic V. Burnstock G. (1998) Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413 492.
49. Resende R. R., Majumder P., Gomes K. N., Britto L. R. Ulrich H. (2007) P19 embryonal carcinoma cells as in vitro model for studying purinergic receptor expression and modulation of N-methyl-D-aspartate-glutamate and acetylcholine receptors during neuronal differentiation. Neuroscience 146, 1169 1181.
50. Roberts J. A., Vial C., Digby H. R., Agboh K. C., Wen H., Atterbury-Thomas A. Evans R. J. (2006) Molecular properties of P2X receptors. Pflügers Arch 452, 486 500.
51. Rodrigues R. J., Almeida T., Richardson P. J., Oliveira C. R. Cunha R. A. (2005) Dual presynaptic control by ATP of glutamate release via facilitatory P2X1, P2X2/3, and P2X3 and inhibitory P2Y1, P2Y2, and/or P2Y4 receptors in the rat hippocampus. J. Neurosci. 25, 6286 6295.
52. Simon J., Filippov A. K., Goransson S., Wong Y. H., Frelin C., Michel A. D., Brown D. A. Barnard E. A. (2002) Characterization and channel coupling of the P2Y(12) nucleotide receptor of brain capillary endothelial cells. J. Biol. Chem. 277, 31390 31400.
53. 3H]-noradrenaline release from the isolated guinea-pig right atrium by P2X-receptors located on axon terminals. Br. J. Pharmacol. 131, 1775 1783.
54. Sperlagh B., Kofalvi A., Deuchars J., Atkinson L., Milligan C. J., Buckley N. J. Vizi E. S. (2002) Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J. Neurochem. 81, 1196 1211.
55. Sperlagh B., Zsilla G., Baranyi M., Illes P. Vizi E. S. (2007a) Purinergic modulation of glutamate release under ischemic-like conditions in the hippocampus. Neuroscience 149, 99 111.
56. Sperlagh B., Heinrich A. Csölle C. (2007b) P2 receptor mediated modulation of neurotransmitter release - an update. Purinergic Signal. 3, 269 284.
57. Suzuki E., Kessler M., Montgomery K. Arai A. C. (2004) Divergent effects of the purinoceptor antagonists suramin and pyridoxal-5′-phosphate-6- (2′-naphtylazo-6′nitro-4′,8′-disulfonate) (PPNDS) on a-amino3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors. Mol. Pharmacol. 66, 1738 1747.
58. Tokuyama Y., Hara M., Jones E. M., Fan Z. Bell G. I. (1995) Cloning of rat and mouse P2Y purinoceptors. Biochem. Biophys. Res. Commun. 211, 211 218.
59. Tonazzini I., Trincavelli M. L., Storm-Mathisen J., Martini C. Bergersen L. H. (2007) Co-localization and functional cross-talk between A1 and P2Y1 purine receptors in rat hippocampus. Eur. J. Neurosci. 26, 890 902.
60. + channel block prevents the ischemia-induced release of norepinephrine from spinal cord slices. Eur. J. Pharmacol. 346, 145 150.
61. 2+)-activated ATP-ase, of acetylcholine release in cortical slices from rat brain. J. Physiol. 226, 95 117.
62. Vizi E. S. (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.
63. Wieraszko A., Goldsmith G. Seyfried T. N. (1989) Stimulation-dependent release of adenosine triphosphate from hippocampal slices. Brain Res. 485, 244 250.
64. Yoshioka K., Saitoh O. Nakata H. (2001) Heteromeric association creates a P2Y-like adenosine receptor. Proc. Natl Acad. Sci. USA 98, 7617 7622.
65. Yoshioka K., Saitoh O. Nakata H. (2002) Agonist-promoted heteromeric oligomerization between adenosine A(1) and P2Y(1) receptors in living cells. FEBS Lett. 523, 147 151.