Elevation of intracellular cAMP evokes activity-dependent release of adenosine in cultured rat forebrain neurons

European Journal of Neuroscience

Volumn 19, Issue 10, 2004, Pages 2669-2681

  Lu, Yin ^a   Li, Ya ^a   Herin, Greta Ann ^b   Aizenman, Elias ^b   Epstein, Paul M ^c   Rosenberg, Paul A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

cGMP; Homeostatic feedback; NMDA; Phosphodiesterase; Plasticity; Zaprinast

Indexed keywords

ADENOSINE; ADENYLATE CYCLASE; AMINOTRANSFERASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIZOCILPINE; FORSKOLIN; GLUTAMIC ACID; ISOENZYME; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PHOSPHODIESTERASE I; PYRUVIC ACID DERIVATIVE; TETRODOTOXIN; VINPOCETINE; ZAPRINAST;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; EXTRACELLULAR SPACE; FOREBRAIN; INTRACELLULAR SPACE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; STATISTICAL SIGNIFICANCE;

ADENOSINE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CYCLIC AMP; CYCLIC GMP; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO; ENZYME ACTIVATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR SPACE; FEMALE; GLUTAMIC ACID; INTRACELLULAR SPACE; MALE; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; N-METHYLASPARTATE; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; PREGNANCY; PROSENCEPHALON; PURINONES; RATS; RATS, SPRAGUE-DAWLEY; THIONUCLEOTIDES;

EID: 2942619041     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0953-816X.2004.03396.x     Document Type: Article

References (79)

1. Ahn, H.S., Crim, W., Pitts, B. & Sybertz, E.J. (1992) Calcium-calmodulin-stimulated and cyclic GMP-specific phosphodiesterases: tissue distribution, drug sensitivity, and regulation of cyclic GMP levels. Advance Second Messenger Phosphoprotein Res., 25, 271-288.
2. Ahn, H.S., Crim, W., Romano, M., Sybertz, E. & Pitts, B. (1989) Effects of selective inhibitors on cyclic nucleotide phosphodiesterases of rabbit aorta. Biochem. Pharmacol., 38, 3331-3339.
3. Andreeva, S.G., Dikkes, P., Epstein, P.M. & Rosenberg, P.A. (2001) Expression of cGMP-specific phosphodiesterase 9A mRNA in the rat brain. J. Neurosci., 21, 9068-9076.
4. Arai, A., Kessler, M. & Lynch, G. (1990) The effects of adenosine on the development of long-term potentiation. Neurosci. Lett., 119, 41-44.
5. Beavo, J.A. (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev., 75, 725-748.
6. Beavo, J.A., Rogers, N.L., Crofford, O.B., Hardman, J.G., Sutherland, E.W. & Newman, E.V. (1970) Effects of xanthine derivatives on lipolysis and on adenosine 3′,5′-monophosphate phosphodiesterase activity. Mol. Pharmacol., 6, 597-603.
7. Bentley, J.K., Kadlecek, A., Sherbert, C.H., Seger, D., Sonnenburg, W.K., Charbonneau, H., Novack, J.P. & Beavo, J.A. (1992) Molecular cloning of cDNA encoding a '63'-kDa calmodulin-stimulated phosphodiesterase from bovine brain. J. Biol. Chem., 267, 18676-18682.
8. Blitzblau, R., Gupta, S., Djali, S., Robinson, M.B. & Rosenberg, P.A. (1996) The glutamate transport inhibitor 1-trans-pyrrolidine-2,4-dicarboxylate indirectly evokes NMDA receptor mediated neurotoxicity in rat cortical cultures. Eur. J. Neurosci., 8, 1840-1852.
9. Bonci, A. & Williams, J.T. (1996) A common mechanism mediates long-term changes in synaptic transmission after chronic cocaine and morphine. Neuron, 16, 631-639.
10. Boulton, C.L., Irving, A.J., Southam, E., Potier, B., Garthwaite, J. & Collingridge, G.L. (1994) The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci., 6, 1528-1535.
11. Bouron, A. & Reuter, H. ( 1999) The D1 dopamine receptor agonist SKF-38393 stimulates the release of glutamate in the hippocampus. Neuroscience, 94, 1063-1070.
12. Broome, M.R., Collingridge, G.L. & Irving, A.J. (1994) Activation of the NO-cGMP signalling pathway depresses hippocampal synaptic transmission through an adenosine receptor-dependent mechanism. Neuropharmacology, 33, 1511-1513.
13. Brunig, I., Sommer, M., Hatt, H. & Bormann, J. (1999) Dopamine receptor subtypes modulate olfactory bulb γ-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. USA, 96, 2456-2460.
14. Burke, L.P. & Nadler, J. V. (1988) Regulation of glutamate and aspartate release from slices of the hippocampal CA1 area: effect of adenosine and baclofen. J. Neurochem., 51, 1541-1551.
15. Calabresi, P., Gubellini, P., Centonze, D., Sancesario, G., Morello, M., Giorgi, M., Pisani, A. & Germardo, G. (1999) A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J. Neurosci., 19, 2489-2499.
16. Carswell, H.V., Graham, D.I. & Stone, T.W. (1997) Kainate-evoked release of adenosine from the hippocampus of the anaesthetised rat: possible involvement of free radicals. J. Neurochem., 68, 240-247.
17. Chen, Y., Graham, D.I. & Stone, T.W. (1992) Release of endogenous adenosine and its metabolites by the activation of NMDA receptors in the rat hippocampus in vivo. Br. J. Pharm., 106, 632-638.
18. Choi, O.H., Shamim, M.T., Padgett, W.L. & Daly, J.W. (1988) Caffeine and theophylline analogues: correlation of behavioral effects with activity as adenosine receptor antagonists and as phosphodiesterase inhibitors. Life Sci., 43, 387-398.
19. Craig, C.G. & White, T.D. (1993) N-methyl-D-aspartate- and non-N-methyl-D-aspartate-evoked adenosine release from rat cortical slices: distinct purinergic sources and mechanisms of release. J. Neurochem., 60, 1073-1080.
20. Cunha, R.A. & Ribeiro, J.A. (2000) Purinergic modulation of [(3) H] GABA release from rat hippocampal nerve terminals. Neuropharmacology, 39, 1156-1167.
21. Curtis, D.R., Duggan, A.W., Felix, D. & Johnston, G.A. (1970) Bicuculline and central GABA receptors. Nature, 228, 676-677.
22. De Mendonca, A. & Ribeiro, J.A. (1990) 2-Chloroadenosine decreases long-term potentiation in the hippocampal CA1 area of the rat. Neurosci. Lett., 118, 107-111.
23. Dolphin, A.C. & Archer, E.R. (1983) An adenosine agonist inhibits and a cyclic AMP analogue enhances the release of glutamate but not GABA from slices of rat dentate gyrus. Neurosci. Lett., 43, 49-54.
24. Dousa, T.P. (1999) Cyclic-3′,5′-nucleotide phosphodiesterase isozymes in cell biology and pathophysiology of the kidney. Kidney Int., 55, 29-62.
25. Evans, D.I., Jones, R.S. & Woodhall, G. (2001) Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex. J. Neurophysiol., 85, 571-579.
26. Evans, G.J. & Morgan, A. (2003) Regulation of the exocytotic machinery by cAMP-dependent protein kinase: implications for presynaptic plasticity. Biochem. Soc. Trans., 31, 824-827.
27. Fawcett, L., Baxendale, R., Stacey, P., McGrouther, C., Harrow, I., Soderling, S., Hetman, J., Beavo, J.A. & Phillips, S.C. (2000) Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc. Natl. Acad. Sci. USA, 97, 3702-3707.
28. Fisher, D.A., Smith, J.F., Pillar, J.S., St Denis, S.H. & Cheng, J.B. (1998) Isolation and characterization of PDE9A, a novel human cGMP-specific phosphodiesterase. J. Biol. Chem., 273, 15559-15564.
29. Fujii, S., Kuroda, Y., Ito, K.L., Yoshioka, M., Kaneko, K., Yamazaki, Y., Sasaki, H. & Kato, H. (2000) Endogenous adenosine regulates the effects of low-frequency stimulation on the induction of potentiation in CA1 neurons of guinea pig hippocampal slices. Neurosci. Lett., 279, 121-124.
30. Garthwaite, J., Southam, E., Boulton, C.L., Nielsen, E.B., Schmidt, K. & Mayer, B. (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol., 48, 184-188.
31. Gereau, R.W. 4th & Conn, P.J. (1994) Potentiation of cAMP responses by metabotropic glutamate receptors depresses excitatory synaptic transmission by a kinase-independent mechanism. Neuron, 12, 1121-1129.
32. Gillespie, P.G. & Beavo, J.A. (1989) Inhibition and stimulation of photoreceptor phosphodiesterase by dipyridamole and M & B 22,948. Mol. Pharmacol., 36, 773-781.
33. Gjertsen, B.T., Mellgren, G., Otten, A., Maronde, E., Genieser, H.G., Jastorff, B., Vintermyr, O.K., McKnight, G.S. & Doskeland, S.O. (1995) Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture: basal cAMP-kinase activity modulates interleukin-1β action. J. Biol. Chem., 270, 20599-20607.
34. Greene, R.W. & Haas, H.L. (1991) The electrophysiology of adenosine in the mammalian central nervous system. Prog. Neurobiol., 36, 329-341.
35. Harris, K.M. & Rosenberg, P.A. (1993) Localization of synapses in rat cortical cultures. Neuroscience, 53, 495-508.
36. Hartell, N.A. (1996) Inhibition of cGMP breakdown promotes the induction of cerebellar long-term depression. J. Neurosci., 16, 2881-2890.
37. Haas, H.L. & Greene, R.W. (1984) Adenosine enhances afterhyperpolarization and accommodation in hippocampal pyramidal cells. Pfluegers. Arch., 402, 244-247.
38. Herrero, I. & Sanchez-Prieto, J. (1996) cAMP-dependent facilitation of glutamate release by beta-adrenergic receptors in cerebrocortical nerve terminals. J. Biol. Chem., 271, 30554-30560.
39. Jackisch, R., Strittmatter, H., Kasakov, L. & Hertting, G. (1984) Endogenous adenosine as a modulator of hippocampal acetylcholine release. Naunyn Shmiedebergs Arch. Pharmacol., 327, 319-325.
40. Johnson, R., Alvarez, R. & Salomon, Y. (1994) Determination of adenylyl cyclase catalytic activity using single and double column procedures. Meth. Enzymol., 238, 31-56.
41. Kotera, J., Yanaka, N., Fujishige, K., Imai, Y., Akatsuka, H., Ishizuka, T., Kawashima, K. & Omori, K. (1997) Expression of rat cGMP-binding cGMP-specific phosphodiesterase mRNA in Purkinje cell layers during postnatal neuronal development. Eur. J. Biochem., 249, 434-442.
42. Kruuse, C., Rybalkin, S.D., Khurana, T.S., Jansen-Olesen, I., Olesen, J. & Edvinsson, L. (2001) The role of cGMP hydrolyzing phosphodiesterases 1 and 5 in cerebral artery dilatation. Eur. J. Pharmacol., 420, 55-65.
43. Lu, Y., Chung, H.J., Li, Y. & Rosenberg, P.A. (2003) NMDA receptor-mediated adenosine accumulation in rat forebrain neurons in culture is associated with inhibition of adenosine kinase. Eur. J. Neurosci., 17, 1213-1222.
44. Lu, Y., Li, Y., Le, M. & Rosenberg, P.A. (1999) The role of cyclic AMP in zaprinast stimulated extracellular adenosine accumulation in rat forebrain neurons. Soc. Neurosci. Abstr., 25, 1615.
45. Manganiello, V.C., Murata, T., Taira, M., Belfrage, P. & Degerman, E. (1995) Diversity in cyclic nucleotide phosphodiesterase isoenzyme families. Arch. Biochem. Biophys., 322, 1-13.
46. Manzoni, O.J., Manabe, T. & Nicoll, R.A. (1994) Release of adenosine by activation of NMDA receptors in the hippocampus. Science, 265, 2098-2101.
47. A receptor β subunits determine regulation by cAMP-dependent protein kinase. Nature Neurosci., 1, 23-28.
48. Melani, A., Corsi, C., Gimenez-Llort, L., Martinez, E., Ogren, S.O., Pedata, F. & Ferre, S. (1999) Effect of N-methyl-D-aspartate on motor activity and in vivo adenosine striatal outflow in the rat. Eur. J. Pharmacol., 385, 15-19.
49. Nicholls, D.G., Sihra, T.S. & Sanchez-Prieto, J. (1987) Calcium-dependent and -independent release of glutamate from synaptosomes monitored by continuous fluorometry. J. Neurochem., 49, 50-57.
50. O'Brien, R.J. & Fischbach, G.D. (1986) Modulation of embryonic chick motoneuron glutamate sensitivity by interneurons and agonists. J. Neurosci., 6, 3290-3296.
51. Pape, H.C. (1992) Adenosine promotes burst activity in guinea-pig geniculocortical neurones through two different ionic mechanisms. J. Physiol. (Lond.), 447, 729-753.
52. Rainnie, D.G., Grunze, H.C., McCarley, R.W. & Greene, R.W. (1994) Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. Science, 263, 689-692.
53. Rosenberg, P.A. (1991) Accumulation of extracellular glutamate and neuronal death in astrocyte-poor cortical cultures exposed to glutamine. Glia, 4, 91-100.
54. Rosenberg, P.A. & Dichter, M.A. (1989) Extracellular cAMP accumulation and degradation in rat cerebral cortex in dissociated cell culture. J. Neurosci., 9, 2654-2663.
55. Rosenberg, P.A., Knowles, R., Knowles, K.P. & Li, Y. (1994) Beta-adrenergic receptor-mediated regulation of extracellular adenosine in cerebral cortex in culture. J. Neurosci., 14, 2953-2965.
56. Rosenberg, P.A. & Li, Y. (1995a) Adenylyl cyclase activation underlies intracellular cyclic AMP accumulation, cyclic AMP transport, and extracellular adenosine accumulation evoked by beta-adrenergic receptor stimulation in mixed cultures of neurons and astrocytes derived from rat cerebral cortex. Brain Res., 692, 227-232.
57. Rosenberg, P.A. & Li, Y. (1995b) Vasoactive intestinal peptide regulates extracellular adenosine levels in rat cortical cultures. Neurosci. Lett., 200, 93-96.
58. Rosenberg, P.A. & Li, Y. (1996) Forskolin evokes extracellular adenosine accumulation in rat cortical cultures. Neurosci. Lett., 211, 49-52.
59. Rosenberg, P.A., Li, Y., Le, M. & Zhang, Y. (2000) Nitric oxide stimulated increase in extracellular adenosine accumulation in rat forebrain in culture is associated with ATP hydrolysis and inhibition of adenosine kinase activity. J. Neurosci., 20, 6294-6301.
60. Salomon, Y. (1979) Adenylate cyclase assay. Adv. Cyclic Nucleotide Res., 10, 35-55.
61. Seamon, K.B., Padgett, W. & Daly, J.W. (1981) Forskolin: unique diterpene activator of adenylate cyclase in membrane and in intact cells. Proc. Natl. Acad. Sci. USA, 78, 3363-3367.
62. Sharma, R.K., Adachi, A.M., Adachi, K. & Wang, J.H. (1984) Demonstration of bovine brain calmodulin-dependent cyclic nucleotide phosphodiesterase isozymes by monoclonal antibodies. J. Biol. Chem., 259, 9248-9254.
63. Sistiaga, A., Miras-Portugal, M.T. & Sanchez-Prieto, J. (1997) Modulation of glutamate release by a nitric oxide/cyclic GMP-dependent pathway. Eur. J. Pharmacol., 321, 247-257.
64. Sonnenburg, W.K., Seger, D. & Beavo, J.A. (1993) Molecular cloning of a cDNA encoding the '61-kDa' calmodulin-stimulated cyclic nucleotide phosphodiesterase. Tissue-specific expression of structurally related isoforms. J. Biol. Chem., 268, 645-652.
65. Sonnenburg, W.K., Seger, D., Kwak, K.S., Huang, J., Charbonneau, H. & Beavo, J.A. (1995) Identification of inhibitory and calmodulin-binding domains of the PDE1A1 and PDE1A2 calmodulin-stimulated cyclic nucleotide phosphodiesterases. J. Biol. Chem., 270, 30989-31000.
66. Staveren, W.V., Itersum, M.M., Steinbusch, H.W.M. & Vente, S.J.D. (2001) The effects of phosphodiesterase inhibition on cyclic GMP and cyclic AMP accumulation in the hippocampus of the rat. Brain Res., 888, 274-286.
67. Suvarna, N.U. & O'Donnell, J.M. (2002) Hydrolysis of N-methyl-D-aspartate receptor-stimulated cAMP and cGMP by PDE4 and PDE2 phosphodiesterases in primary neuronal cultures of rat cerebral cortex and hippocampus. J. Pharm. Exp. Ther., 302, 249-256.
68. Trussel, L.O. & Jackson, M.B. (1987) Dependence of an adenosine-activated potassium current on a GTP-binding protein in mammalian central neurons. J. Neurosci., 7, 3306-3316.
69. Wang, G.J., Chung, H.J., Schnuer, J., Lea, E., Robinson, M.B., Potthoff, W.K., Aizenman, E. & Rosenberg, P.A. (1998) Dihydrokainate-sensitive neuronal glutamate transport is required for protection of rat cortical neurons in culture against synaptically released glutamate. Eur. J. Neurosci., 10, 2523-2531.
70. Wang, H.L., Li, A. & Wu, T. (1997) Vasoactive intestinal polypeptide enhances the GABAergic synaptic transmission in cultured hippocampal neurons. Brain Res., 746, 294-300.
71. Wei, J.Y., Han, M.H., Cohen, E.D. & Barnstable, C.J. (1999) cGMP selectively silences GABAergic synapses in visual cortical neurons through a presynaptic mechanism. Soc. Neurosci. Abstr., 25, 2189.
72. Wei, J., Jin, X., Cohen, E.D., Daw, N.W. & Barnstable, C.J. (2002) cGMP-induced presynaptic depression and postsynaptic facilitation at glutamatergic synapses in visual cortex. Brain Res., 927, 42-54.
73. Weiss, S. (1988) Forskolin attenuates the evoked release of [3H] GABA from striatal neurons in primary culture. Brain Res., 463, 182-186.
74. Wells, J.N., Wu, Y.J., Baird, C.E. & Hardman, J.G. (1975) Phosphodiesterases from porcine coronary arteries: inhibition of separated forms by xanthines, papaverine, and cyclic nucleotides. Mol. Pharmacol., 11, 775-783.
75. West, A.E., Griffith, E.C. & Greenberg, M.E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci., 12, 921-931.
76. Yamashita, N., Yamauchi, M., Baba, J. & Sawa, A. (1997) Phosphodiesterase type 4 that regulates cAMP level in cortical neurons shows high sensitivity to rolipram. Eur. J. Pharmacol., 337, 95-102.
77. Yan, C., Zhao, A.Z., Bentley, J.K. & Beavo, J.A. (1996) The calmodulin-dependent phosphodiesterase gene PDE1C encodes several functionally different splice variants in a tissue-specific manner. J. Biol. Chem., 271, 25699-25706.
78. Yan, C., Zhao, A.Z., Bentley, J.K., Loughney, K., Ferguson, K. & Beavo, J.A. (1995) Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA, 92, 9677-9681.
79. Yu, W. & Miller, R.F. (1994) NBQX suppresses inhibitory glycine currents in retinal ganglion cells. Neuroreport, 5, 1558-1560.