Adenosine inhibits paraventricular pre-sympathetic neurons through ATP-dependent potassium channels

Journal of Neurochemistry

Volumn 113, Issue 2, 2010, Pages 530-542

  Li, De Pei ^a   Chen, Shao Rui ^a   Pan, Hui Lin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Adenosine receptors; G proteins; Hypothalamus; KATP; Sympathetic nervous system; Synaptic transmission

Indexed keywords

8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GLIBENCLAMIDE; GUANOSINE 5' O (2 THIODIPHOSPHATE); TOLBUTAMIDE;

ADRENERGIC TRANSMISSION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTERIOR HYPOTHALAMUS; ARTICLE; CONTROLLED STUDY; HYPERPOLARIZATION; IMMUNOCYTOCHEMISTRY; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SYMPATHETIC NERVE CELL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ADENOSINE; ANALGESICS; ANIMALS; BICUCULLINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GLYBURIDE; GUANOSINE DIPHOSPHATE; KATP CHANNELS; MALE; MEMBRANE POTENTIALS; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ADENOSINE A1; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; THIONUCLEOTIDES; TOLBUTAMIDE; TRIAZINES; TRIAZOLES; XANTHINES;

RATTUS;

EID: 77949687475     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06618.x     Document Type: Article

References (61)

1. Allen A. M. (2002) Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 39, 275 280.
2. Andoh T., Ishiwa D., Kamiya Y., Echigo N., Goto T. Yamada Y. (2006) A1 adenosine receptor-mediated modulation of neuronal ATP-sensitive K channels in rat substantia nigra. Brain Res. 1124, 55 61.
3. + channels. Trends Neurosci. 21, 288 294.
4. Bagley E. E., Vaughan C. W. Christie M. J. (1999) Inhibition by adenosine receptor agonists of synaptic transmission in rat periaqueductal grey neurons. J. Physiol. 516 (Pt 1), 219 225.
5. Ballarin M., Fredholm B. B., Ambrosio S. Mahy N. (1991) Extracellular levels of adenosine and its metabolites in the striatum of awake rats: Inhibition of uptake and metabolism. Acta Physiol. Scand. 142, 97 103.
6. + channel activation as revealed by hydrolysis-resistant GTP analogues. J. Gen. Physiol. 91, 469 493.
7. Chamberlin N. L., Arrigoni E., Chou T. C., Scammell T. E., Greene R. W. Saper C. B. (2003) Effects of adenosine on gabaergic synaptic inputs to identified ventrolateral preoptic neurons. Neuroscience 119, 913 918.
8. Corradetti R., Lo Conte G., Moroni F., Passani M. B. Pepeu G. (1984) Adenosine decreases aspartate and glutamate release from rat hippocampal slices. Eur. J. Pharmacol. 104, 19 26.
9. Cunha R. A., Constantino M. D. Ribeiro J. A. (1997) ZM241385 is an antagonist of the facilitatory responses produced by the A2A adenosine receptor agonists CGS21680 and HENECA in the rat hippocampus. Br. J. Pharmacol. 122, 1279 1284.
10. Dart C. Standen N. B. (1993) Adenosine-activated potassium current in smooth muscle cells isolated from the pig coronary artery. J. Physiol. 471, 767 786.
11. Dixon A. K., Gubitz A. K., Sirinathsinghji D. J., Richardson P. J. Freeman T. C. (1996) Tissue distribution of adenosine receptor mRNAs in the rat. Br. J. Pharmacol. 118, 1461 1468.
12. Dunwiddie T. V. Fredholm B. B. (1989) Adenosine A1 receptors inhibit adenylate cyclase activity and neurotransmitter release and hyperpolarize pyramidal neurons in rat hippocampus. J. Pharmacol. Exp. Ther. 249, 31 37.
13. Dunwiddie T. V. Masino S. A. (2001) The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31 55.
14. Dunwiddie T. V., Diao L. Proctor W. R. (1997) Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J. Neurosci. 17, 7673 7682.
15. Fastbom J., Pazos A. Palacios J. M. (1987) The distribution of adenosine A1 receptors and 5′-nucleotidase in the brain of some commonly used experimental animals. Neuroscience 22, 813 826.
16. Feuerstein T. J., Hertting G. Jackisch R. (1985) Modulation of hippocampal serotonin (5-HT) release by endogenous adenosine. Eur. J. Pharmacol. 107, 233 242.
17. Feuerstein T. J., Bar K. I. Lucking C. H. (1988) Activation of A1 adenosine receptors decreases the release of serotonin in the rabbit hippocampus, but not in the caudate nucleus. Naunyn Schmiedebergs Arch. Pharmacol. 338, 664 670.
18. Fredholm B. B., AP I. J., Jacobson K. A., Klotz K. N. Linden J. (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53, 527 552.
19. Gilman A. G. (1987) G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615 649.
20. Ginsborg B. L. Hirst G. D. (1972) The effect of adenosine on the release of the transmitter from the phrenic nerve of the rat. J. Physiol. 224, 629 645.
21. Gross G. J. Auchampach J. A. (1992) Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ. Res. 70, 223 233.
22. Hardy S. G. (2001) Hypothalamic projections to cardiovascular centers of the medulla. Brain Res. 894, 233 240.
23. Hepler J. R. Gilman A. G. (1992) G proteins. Trends Biochem. Sci. 17, 383 387.
24. + channels in cerebral ischemic preconditioning. Proc. Natl Acad. Sci. USA 92, 4666 4670.
25. + channels in excised membrane patches is mediated by PKC. Am. J. Physiol. 276, H488 H495.
26. Jeong H. J., Jang I. S., Nabekura J. Akaike N. (2003) Adenosine A1 receptor-mediated presynaptic inhibition of GABAergic transmission in immature rat hippocampal CA1 neurons. J. Neurophysiol. 89, 1214 1222.
27. + channels. Biochemistry 37, 13291 13299.
28. + channels to A1 receptors by G proteins in rat ventricular myocytes. Am. J. Physiol. 259, H820 H826.
29. Laborit H., Manzo-Fay G., Baron C. Hasni H. (1990) Changes in plasma catecholamine levels after the intraperitoneal and intracerebroventricular administration of adenosine analogues and of clonidine in conscious rats. Res. Commun. Chem. Pathol. Pharmacol. 68, 307 327.
30. Latini S. Pedata F. (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem. 79, 463 484.
31. Latini S., Corsi C., Pedata F. Pepeu G. (1995) The source of brain adenosine outflow during ischemia and electrical stimulation. Neurochem. Int. 27, 239 244.
32. Li D. P., Chen S. R., Finnegan T. F. Pan H. L. (2004) Signalling pathway of nitric oxide in synaptic GABA release in the rat paraventricular nucleus. J. Physiol. 554, 100 110.
33. Li D. P., Yang Q., Pan H. M. Pan H. L. (2008a) Plasticity of pre- and postsynaptic GABAB receptor function in the paraventricular nucleus in spontaneously hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 295, H807 H815.
34. Li D. P., Yang Q., Pan H. M. Pan H. L. (2008b) Pre- and postsynaptic plasticity underlying augmented glutamatergic inputs to hypothalamic presympathetic neurons in spontaneously hypertensive rats. J. Physiol. 586, 1637 1647.
35. + channels. A possible mechanistic link to ischemic preconditioning. Circ. Res. 79, 399 406.
36. Lohse M. J., Klotz K. N., Lindenborn-Fotinos J., Reddington M., Schwabe U. Olsson R. A. (1987) 8-Cyclopentyl-1,3-dipropylxanthine (DPCPX) - a selective high affinity antagonist radioligand for A1 adenosine receptors. Naunyn Schmiedebergs Arch. Pharmacol. 336, 204 210.
37. Mironov S. L., Langohr K. Richter D. W. (1999) A1 adenosine receptors modulate respiratory activity of the neonatal mouse via the cAMP-mediated signaling pathway. J. Neurophysiol. 81, 247 255.
38. Mitchell J. B., Lupica C. R. Dunwiddie T. V. (1993) Activity-dependent release of endogenous adenosine modulates synaptic responses in the rat hippocampus. J. Neurosci. 13, 3439 3447.
39. Miyakubo H., Hayashi Y. Tanaka J. (2002) Enhanced response of subfornical organ neurons projecting to the hypothalamic paraventricular nucleus to angiotensin II in spontaneously hypertensive rats. Auton. Neurosci. 95, 131 136.
40. Nakatsuka T., Fujita T., Inoue K. Kumamoto E. (2008) Activation of GIRK channels in substantia gelatinosa neurones of the adult rat spinal cord: a possible involvement of somatostatin. J. Physiol. 586, 2511 2522.
41. Oliet S. H. Poulain D. A. (1999) Adenosine-induced presynaptic inhibition of IPSCs and EPSCs in rat hypothalamic supraoptic nucleus neurones. J. Physiol. 520 (Pt 3), 815 825.
42. Oliveira J. C., Sebastiao A. M. Ribeiro J. A. (1991) Solubilized rat brain adenosine receptors have two high-affinity binding sites for 1,3-dipropyl-8-cyclopentylxanthine. J. Neurochem. 57, 1165 1171.
43. Ponzio T. A. Hatton G. I. (2005) Adenosine postsynaptically modulates supraoptic neuronal excitability. J. Neurophysiol. 93, 535 547.
44. Ponzio T. A., Wang Y. F. Hatton G. I. (2006) Activation of adenosine A2A receptors alters postsynaptic currents and depolarizes neurons of the supraoptic nucleus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R359 R366.
45. Pyner S. Coote J. H. (2000) Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 100, 549 556.
46. Ranson R. N., Motawei K., Pyner S. Coote J. H. (1998) The paraventricular nucleus of the hypothalamus sends efferents to the spinal cord of the rat that closely appose sympathetic preganglionic neurones projecting to the stellate ganglion. Exp. Brain Res. 120, 164 172.
47. Rebola N., Lujan R., Cunha R. A. Mulle C. (2008) Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron 57, 121 134.
48. Ross E. M. (1989) Signal sorting and amplification through G protein-coupled receptors. Neuron 3, 141 152.
49. Sebastiao A. M., Stone T. W. Ribeiro J. A. (1990) The inhibitory adenosine receptor at the neuromuscular junction and hippocampus of the rat: antagonism by 1,3,8-substituted xanthines. Br. J. Pharmacol. 101, 453 459.
50. Shan H. Q. Cheng J. S. (2000) Effect of adenosine on adenosine triphosphate-sensitive potassium channel during hypoxia in rat hippocampal neurons. Neurosci. Lett. 286, 45 48.
51. Stehle J. H., Rivkees S. A., Lee J. J., Weaver D. R., Deeds J. D. Reppert S. M. (1992) Molecular cloning and expression of the cDNA for a novel A2-adenosine receptor subtype. Mol. Endocrinol. 6, 384 393.
52. Stella L., Berrino L., Maione S., de Novellis V. Rossi F. (1993) Cardiovascular effects of adenosine and its analogs in anaesthetized rats. Life Sci. 53, 755 763.
53. Swanson L. W. Sawchenko P. E. (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev. Neurosci. 6, 269 324.
54. Thompson S. M., Haas H. L. Gahwiler B. H. (1992) Comparison of the actions of adenosine at pre- and postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 451, 347 363.
55. Tseng G. F., Parada I. Prince D. A. (1991) Double-labelling with rhodamine beads and biocytin: a technique for studying corticospinal and other projection neurons in vitro. J. Neurosci. Methods 37, 121 131.
56. de Wardener H. E. (2001) The hypothalamus and hypertension. Physiol. Rev. 81, 1599 1658.
57. White T. D. Hoehn K. (1991) Release of adenosine and ATP from nervous tissue, in Adenosine in the Nervous System (Stone T. W., ed pp. 173 195. London Academic Press, London.
58. Yang Q., Chen S. R., Li D. P. Pan H. L. (2007) Kv1.1/1.2 channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience 149, 315 327.
59. Yoon K. W. Rothman S. M. (1991) Adenosine inhibits excitatory but not inhibitory synaptic transmission in the hippocampus. J. Neurosci. 11, 1375 1380.
60. Zhang W., Carreno F. R., Cunningham J. T. Mifflin S. W. (2008) Chronic sustained and intermittent hypoxia reduce function of ATP-sensitive potassium channels in nucleus of the solitary tract. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1555 R1562.
61. Zocchi C., Ongini E., Ferrara S., Baraldi P. G. Dionisotti S. (1996) Binding of the radioligand [3H]-SCH 58261, a new non-xanthine A2A adenosine receptor antagonist, to rat striatal membranes. Br. J. Pharmacol. 117, 1381 1386.