From A 1 to A 3 en passant through A 2A receptors in the hippocampus: Pharmacological implications

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 6, 2012, Pages 652-663

  Sebastião, Ana M ^a   Ribeiro, Filipa F ^a   Ribeiro, Joaquim A ^a  

^a UNIVERSITY OF LISBON   (Portugal)

Author keywords

aminobutyric acid; Adenosine receptors; Brain derived neurotrophic factor; Cannabinoids; Glutamate; Hippocampus; Neuroprotection; Vasoactive intestinal peptide

Indexed keywords

ACETYLCHOLINE; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A3 RECEPTOR; AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE RELATED PEPTIDE; CANNABINOID; CANNABINOID RECEPTOR; GLUTAMIC ACID; INTERLEUKIN 6; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NORADRENALIN; REACTIVE OXYGEN METABOLITE; SEROTONIN; VASOACTIVE INTESTINAL POLYPEPTIDE; GLUTAMATE RECEPTOR;

ARTICLE; HIPPOCAMPUS; HUMAN; HYPOTHERMIA; HYPOXIA; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NEUROTRANSMITTER UPTAKE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR INTRINSIC ACTIVITY; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY; REVIEW;

ADENOSINE; ANIMALS; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A3; RECEPTORS, GLUTAMATE;

EID: 84869024880     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152712803581074     Document Type: Article

References (137)

1. Daly, J.W. Role of cyclic nucleotides in the nervous system, in: Handbook of Psychopharmacology; Iversen, L.L.; Iversen, S.D.; Snyder, S.H., Ed.; Plenum Press: New York, 1975; Vol. 5, pp. 47-130.
2. Dunwiddie, T.V.; Hoffer, B.J. Adenine nucleotides and synaptic transmission in the in vitro rat hippocampus. Br. J. Pharmacol., 1980, 69(1), 59-68.
3. Ribeiro, J.A.; Sebastião, A.M. Modulation and metamodulation of synapses by adenosine. Acta Physiol. (Oxf.), 2010, 199(2), 161-169.
4. Sebastião, A.M.; Ribeiro, J.A. Fine-tuning neuromodulation by adenosine. Trends Pharmacol. Sci., 2000, 21(9), 341-6.
5. Sebastião, A.M.; Ribeiro, J.A. Tuning and fine-tuning of synapses with adenosine. Curr. Neuropharmacol., 2009, 7(3), 180-194.
6. Sebastião, A.M.; Ribeiro, J.A. Adenosine receptors and the central nervous system. Handb. Exp. Pharmacol., 2009, (193), 471-534.
7. Drury, A.N.; Szent-Gyorgyi, A. The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J. Physiol., 1929, 68(3), 213-237.
8. Dunwiddie, T.V.; Masino, S.A. The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci., 2001, 24, 31-55.
9. Latini, S.; Pedata, F. Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem., 2001, 79(3), 463-484.
10. Zimmermann, H. Ectonucleotidases in the nervous system. Novartis Found. Symp., 2006, 276, 113-128; discussion 128-30, 233-237, 275-281.
11. Boison, D.; Masino, S.A.; Geiger, J.D. Homeostatic bioenergetic network regulation-a novel concept to avoid pharmacoresistance in epilepsy. Expert Opin. Drug Discov., 2011, 6(7), 713-724.
12. Sebastião, A.M.; Cristóvão-Ferreira, S.; Ribeiro, J.A. Downstream Pathways of Adenosine, in: Adenosine: A Key Link between Metabolism and Brain Activity; Masino, S.A.; Boison, D., Ed.; Springer: New York, 2012.
13. Cunha, R.A.; Sebastião, A.M.; Ribeiro, J.A. Inhibition by ATP of hippocampal synaptic transmission requires localized extracellular catabolism by ecto-nucleotidases into adenosine and channeling to adenosine A1 receptors. J. Neurosci., 1998, 18(6), 1987-1995.
14. Heinrich, A.; Andó, R.; Túri, G.; Rózsa, B.; Sperlágh, B. K(+) depolarization evokes ATP, adenosine and glutamate release from glia in rat hippocampus: a microelectrode biosensor study. Br. J. Pharmacol., 2012.
15. Pankratov, Y.; Lalo, U.; Krishtal, O.A.; Verkhratsky, A. P2X receptors and synaptic plasticity. Neuroscience, 2009, 158(1), 137-148.
16. Sebastião, A.M.; Ribeiro, J.A. Triggering neurotrophic factor actions through adenosine A2A receptor activation: implications for neuroprotection. Br. J. Pharmacol., 2009, 158(1), 15-22.
17. Correia-de-Sá, P.; Sebastião, A.M.; Ribeiro, J.A. Inhibitory and excitatory effects of adenosine receptor agonists on evoked transmitter release from phrenic nerve ending of the rat. Br. J. Pharmacol., 1991, 103(2), 1614-1620.
18. Ciruela, F.; Casadó, V.; Rodrigues, R.J.; Luján, R.; Burgueño, J.; Canals, M.; Borycz, J.; Rebola, N.; Goldberg, S.R.; Mallol, J.; Cortés, A.; Canela, E.I.; López-Giménez, J.F.; Milligan, G.; Lluis, C.; Cunha, R.A.; Ferré, S.; Franco, R. Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. J. Neurosci., 2006, 26(7), 2080-2087.
19. Cunha, R.A.; Correia-de-Sá, P.; Sebastião, A.M.; Ribeiro, J.A. Preferential activation of excitatory adenosine receptors at rat hippocampal and neuromuscular synapses by adenosine formed from released adenine nucleotides. Br. J. Pharmacol., 1996, 119(2), 253-260.
20. Jackisch, R.; Strittmatter, H.; Kasakov, L.; Hertting, G. Endogenous adenosine as a modulator of hippocampal acetylcholine release. Naunyn Schmiedebergs Arch. Pharmacol., 1984, 327(4), 319-325.
21. Feuerstein, T.J.; Hertting, G.; Jackisch, R. Modulation of hippocampal serotonin (5-HT) release by endogenous adenosine. Eur. J. Pharmacol., 1985, 107(2), 233-242.
22. Jackisch, R.; Fehr, R.; Hertting, G. Adenosine: an endogenous modulator of hippocampal noradrenaline release. Neuropharmacology, 1985, 24(6), 499-507.
23. Ribeiro, J.A. Purinergic inhibition of neurotransmitter release in the central nervous system. Pharmacol. Toxicol., 1995, 77(5), 299-305.
24. Pinto-Duarte, A.; Coelho, J.E.; Cunha, R.A.; Ribeiro, J.A.; Sebastião, A.M. Adenosine A2A receptors control the extracellular levels of adenosine through modulation of nucleoside transporters activity in the rat hippocampus. J. Neurochem., 2005, 93(3), 595-604.
25. de Mendonça, A.; Sebastião, A.M.; Ribeiro, J.A. Inhibition of NMDA receptor-mediated currents in isolated rat hippocampal neurones by adenosine A1 receptor activation. Neuroreport, 1995, 6(8), 1097-1100.
26. Dias, R.B.; Ribeiro, J.A.; Sebastião, A.M. Enhancement of AMPA currents and GluR1 membrane expression through PKA-coupled adenosine A(2A) receptors. Hippocampus, 2012, 22(2), 276-291.
27. O'Kane, E.M.; Stone, T.W. Interaction between adenosine A1 and A2 receptor-mediated responses in the rat hippocampus in vitro. Eur. J. Pharmacol., 1998, 362(1), 17-25.
28. Sebastião, A.M.; Ribeiro, J.A. Evidence for the presence of excitatory A2 adenosine receptors in the rat hippocampus. Neurosci. Lett., 1992, 138(1), 41-44.
29. Lopes, L.V.; Cunha, R.A.; Kull, B.; Fredholm, B.B.; Ribeiro, J.A. Adenosine A(2A) receptor facilitation of hippocampal synaptic transmission is dependent on tonic A(1) receptor inhibition. Neuroscience, 2002, 112(2), 319-329.
30. Cunha, R.A.; Johansson, B.; van der Ploeg, I.; Sebastião, A.M.; Ribeiro, J.A.; Fredholm, B.B. Evidence for functionally important adenosine A2a receptors in the rat hippocampus. Brain Res., 1994, 649(1-2), 208-216.
31. Lopes, L.V.; Cunha, R.A.; Ribeiro, J.A. Cross talk between A(1) and A(2A) adenosine receptors in the hippocampus and cortex of young adult and old rats. J. Neurophysiol., 1999, 82(6), 3196-3203.
32. Cristóvão-Ferreira, S.; Vaz, S.H.; Ribeiro, J.A.; Sebastião, A.M. Adenosine A2A receptors enhance GABA transport into nerve terminals by restraining PKC inhibition of GAT-1. J. Neurochem., 2009, 109(2), 336-347.
33. Cunha, R.A.; Ribeiro, J.A. Purinergic modulation of [(3)H]GABA release from rat hippocampal nerve terminals. Neuropharmacology, 2000, 39(7), 1156-1167.
34. Rodrigues, R.J.; Canas, P.M.; Lopes, L.V.; Oliveira, C.R.; Cunha, R.A. Modification of adenosine modulation of acetylcholine release in the hippocampus of aged rats. Neurobiol. Aging, 2008, 29(10), 1597-1601.
35. Diógenes, M.J.; Assaife-Lopes, N.; Pinto-Duarte, A.; Ribeiro, J.A.; Sebastião, A.M. Influence of age on BDNF modulation of hippocampal synaptic transmission: interplay with adenosine A2A receptors. Hippocampus, 2007, 17(7), 577-585.
36. Diógenes, M.J.; Fernandes, C.C.; Sebastião, A.M.; Ribeiro, J.A. Activation of adenosine A2A receptor facilitates brain-derived neurotrophic factor modulation of synaptic transmission in hippocampal slices. J. Neurosci., 2004, 24(12), 2905-2913.
37. Fontinha, B.M.; Diógenes, M.J.; Ribeiro, J.A.; Sebastião, A.M. Enhancement of long-term potentiation by brain-derived neurotrophic factor requires adenosine A2A receptor activation by endogenous adenosine. Neuropharmacology, 2008, 54(6), 924-933.
38. Nishizaki, T.; Nagai, K.; Nomura, T.; Tada, H.; Kanno, T.; Tozaki, H.; Li, X.X.; Kondoh, T.; Kodama, N.; Takahashi, E.; Sakai, N.; Tanaka, K.; Saito, N. A new neuromodulatory pathway with a glial contribution mediated via A(2a) adenosine receptors. Glia, 2002, 39(2), 133-147.
39. Matos, M.; Augusto, E.; Santos-Rodrigues, A.D.; Schwarzschild, M.A.; Chen, J.F.; Cunha, R.A.; Agostinho, P. Adenosine A(2A) receptors modulate glutamate uptake in cultured astrocytes and gliosomes. Glia, 2012, 60(5), 702-716.
40. Coelho, J.E.; Rebola, N.; Fragata, I.; Ribeiro, J.A.; de Mendonça, A.; Cunha, R.A. Hypoxia-induced desensitization and internalization of adenosine A1 receptors in the rat hippocampus. Neuroscience, 2006, 138(4), 1195-1203.
41. Fredholm, B.B. Adenosine and neuroprotection. Int. Rev. Neurobiol., 1997, 40, 259-280.
42. Lopes, L.V.; Cunha, R.A.; Ribeiro, J.A. Increase in the number, G protein coupling, and efficiency of facilitatory adenosine A2A receptors in the limbic cortex, but not striatum, of aged rats. J. Neurochem., 1999, 73(4), 1733-1738.
43. Dunwiddie, T.V.; Diao, L.; Kim, H.O.; Jiang, J.L.; Jacobson, K.A. Activation of hippocampal adenosine A3 receptors produces a desensitization of A1 receptor-mediated responses in rat hippocampus. J. Neurosci., 1997, 17(2), 607-614.
44. Macek, T.A.; Schaffhauser, H.; Conn, P.J. Protein kinase C and A3 adenosine receptor activation inhibit presynaptic metabotropic glutamate receptor (mGluR) function and uncouple mGluRs from GTP-binding proteins. J. Neurosci., 1998, 18(16), 6138-6146.
45. Pugliese, A.M.; Coppi, E.; Volpini, R.; Cristalli, G.; Corradetti, R.; Jeong, L.S.; Jacobson, K.A.; Pedata, F. Role of adenosine A3 receptors on CA1 hippocampal neurotransmission during oxygenglucose deprivation episodes of different duration. Biochem. Pharmacol., 2007, 74(5), 768-779.
46. Dennis, S.H.; Jaafari, N.; Cimarosti, H.; Hanley, J.G.; Henley, J.M.; Mellor, J.R. Oxygen/glucose deprivation induces a reduction in synaptic AMPA receptors on hippocampal CA3 neurons mediated by mGluR1 and adenosine A3 receptors. J. Neurosci., 2011, 31(33), 11941-11952.
47. Zhu, C.B.; Steiner, J.A.; Munn, J.L.; Daws, L.C.; Hewlett, W.A.; Blakely, R.D. Rapid stimulation of presynaptic serotonin transport by A(3) adenosine receptors. J. Pharmacol. Exp. Ther., 2007, 322(1), 332-340.
48. de Mendonça, A.; Ribeiro, J.A. Adenosine inhibits the NMDA receptor-mediated excitatory postsynaptic potential in the hippocampus. Brain Res., 1993, 606(2), 351-356.
49. Canhão, P.; de Mendonça, A.; Ribeiro, J.A. 1,3-Dipropyl-8-cyclopentylxanthine attenuates the NMDA response to hypoxia in the rat hippocampus. Brain Res., 1994, 661(1-2), 265-273.
50. Costenla, A.R.; de Mendonça, A.; Sebastião, A.; Ribeiro, J.A. An adenosine analogue inhibits NMDA receptor-mediated responses in bipolar cells of the rat retina. Exp. Eye Res., 1999, 68(3), 367-370.
51. Pamenter, M.E.; Shin, D.S.; Buck, L.T. Adenosine A1 receptor activation mediates NMDA receptor activity in a pertussis toxinsensitive manner during normoxia but not anoxia in turtle cortical neurons. Brain Res., 2008, 1213, 27-34.
52. Sebastião, A.M.; de Mendonça, A.; Moreira, T.; Ribeiro, J.A. Activation of synaptic NMDA receptors by action potentialdependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation. J. Neurosci., 2001, 21(21), 8564-8571.
53. Deng, Q.; Terunuma, M.; Fellin, T.; Moss, S.J.; Haydon, P.G. Astrocytic activation of A1 receptors regulates the surface expression of NMDA receptors through a Src kinase dependent pathway. Glia, 2011, 59(7), 1084-1093.
54. Pietersen, A.N.; Lancaster, D.M.; Patel, N.; Hamilton, J.B.; Vreugdenhil, M. Modulation of gamma oscillations by endogenous adenosine through A1 and A2A receptors in the mouse hippocampus. Neuropharmacology, 2009, 56(2), 481-492.
55. Schulz, S.B.; Klaft, Z.J.; Rosler, A.R.; Heinemann, U.; Gerevich, Z. Purinergic P2X, P2Y and adenosine receptors differentially modulate hippocampal gamma oscillations. Neuropharmacology, 2012, 62(2), 914-924.
56. Bartos, M.; Vida, I.; Jonas, P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci., 2007, 8(1), 45-56.
57. Barry, R.J.; Clarke, A.R.; Johnstone, S.J.; Brown, C.R.; Bruggemann, J.M.; van Rijbroek, I. Caffeine effects on restingstate arousal in children. Int. J. Psychophysiol., 2009, 73(3), 355-361.
58. de Mendonça, A.; Ribeiro, J.A. Influence of metabotropic glutamate receptor agonists on the inhibitory effects of adenosine A1 receptor activation in the rat hippocampus. Br. J. Pharmacol., 1997, 121(8), 1541-1548.
59. de Mendonça, A.; Ribeiro, J.A. Contribution of metabotropic glutamate receptors to the depression of excitatory postsynaptic potentials during hypoxia. Neuroreport, 1997, 8(17), 3667-3671.
60. Rebola, N.; Lujan, R.; Cunha, R.A.; Mulle, C. Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron, 2008, 57(1), 121-134.
61. Cabello, N.; Gandia, J.; Bertarelli, D.C.; Watanabe, M.; Lluis, C.; Franco, R.; Ferre, S.; Lujan, R.; Ciruela, F. Metabotropic glutamate type 5, dopamine D2 and adenosine A2a receptors form higherorder oligomers in living cells. J. Neurochem., 2009, 109(5), 1497-1507.
62. Kachroo, A.; Orlando, L.R.; Grandy, D.K.; Chen, J.F.; Young, A.B.; Schwarzschild, M.A. Interactions between metabotropic glutamate 5 and adenosine A2A receptors in normal and parkinsonian mice. J. Neurosci., 2005, 25(45), 10414-10419.
63. Lisman, J.E.; Grace, A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron, 2005, 46(5), 703-713.
64. Citri, A.; Malenka, R.C. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology, 2008, 33(1), 18-41.
65. Blundon, J.A.; Zakharenko, S.S. Dissecting the components of long-term potentiation. Neuroscientist, 2008, 14(6), 598-608.
66. Arai, A.; Lynch, G. Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation. Brain Res., 1992, 598(1-2), 173-184.
67. de Mendonça, A.; Ribeiro, J.A. Endogenous adenosine modulates long-term potentiation in the hippocampus. Neuroscience, 1994, 62(2), 385-390.
68. Forghani, R.; Krnjevic, K. Adenosine antagonists have differential effects on induction of long-term potentiation in hippocampal slices. Hippocampus, 1995, 5(1), 71-77.
69. de Mendonça, A.; Costenla, A.R.; Ribeiro, J.A. Persistence of the neuromodulatory effects of adenosine on synaptic transmission after long-term potentiation and long-term depression. Brain Res., 2002, 932(1-2), 56-60.
70. Collingridge, G.L.; Kehl, S.J.; McLennan, H. Excitatory amino acids in synaptic transmission in the Schaffer collateralcommissural pathway of the rat hippocampus. J. Physiol., 1983, 334, 33-46.
71. Rex, C.S.; Kramar, E.A.; Colgin, L.L.; Lin, B.; Gall, C.M.; Lynch, G. Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J. Neurosci., 2005, 25(25), 5956-5966.
72. Costenla, A.R.; Diógenes, M.J.; Canas, P.M.; Rodrigues, R.J.; Nogueira, C.; Maroco, J.; Agostinho, P.M.; Ribeiro, J.A.; Cunha, R.A.; de Mendonça, A. Enhanced role of adenosine A(2A) receptors in the modulation of LTP in the rat hippocampus upon ageing. Eur. J. Neurosci., 2011, 34(1), 12-21.
73. Fontinha, B.M.; Delgado-García, J.M.; Madronal, N.; Ribeiro, J.A.; Sebastião, A.M.; Gruart, A. Adenosine A(2A) receptor modulation of hippocampal CA3-CA1 synapse plasticity during associative learning in behaving mice. Neuropsychopharmacology, 2009, 34(7), 1865-1874.
74. Diógenes, M.J.; Costenla, A.R.; Lopes, L.V.; Jerónimo-Santos, A.; Sousa, V.C.; Fontinha, B.M.; Ribeiro, J.A.; Sebastião, A.M. Enhancement of LTP in aged rats is dependent on endogenous BDNF. Neuropsychopharmacology, 2011, 36(9), 1823-1836.
75. de Mendonça, A.; Ribeiro, J.A. Long-term potentiation observed upon blockade of adenosine A1 receptors in rat hippocampus is Nmethyl-D-aspartate receptor-dependent. Neurosci. Lett., 2000, 291(2), 81-84.
76. Colgin, L.L.; Kubota, D.; Jia, Y.; Rex, C.S.; Lynch, G. Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves. J. Physiol., 2004, 558(Pt 3), 953-961.
77. Costenla, A.R.; Lopes, L.V.; de Mendonça, A.; Ribeiro, J.A. A functional role for adenosine A3 receptors: modulation of synaptic plasticity in the rat hippocampus. Neurosci. Lett., 2001, 302(1), 53-57.
78. Almeida, T.; Rodrigues, R.J.; de Mendonça, A.; Ribeiro, J.A.; Cunha, R.A. Purinergic P2 receptors trigger adenosine release leading to adenosine A2A receptor activation and facilitation of long-term potentiation in rat hippocampal slices. Neuroscience, 2003, 122(1), 111-121.
79. de Mendonça, A.; Almeida, T.; Bashir, Z.I.; Ribeiro, J.A. Endogenous adenosine attenuates long-term depression and depotentiation in the CA1 region of the rat hippocampus. Neuropharmacology, 1997, 36(2), 161-167.
80. Márquez-Ruiz, J.; Leal-Campanario, R.; Sánchez-Campusano, R.; Molaee-Ardekani, B.; Wendling, F.; Miranda, P.C.; Ruffini, G.; Gruart, A.; Delgado-García, J.M. Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc. Natl. Acad. Sci. USA, 2012, 109(17), 6710-6715.
81. Lucchi, R.; Latini, S.; de Mendonça, A.; Sebastião, A.M.; Ribeiro, J.A. Adenosine by activating A1 receptors prevents GABAAmediated actions during hypoxia in the rat hippocampus. Brain Res., 1996, 732(1-2), 261-266.
82. Fragata, I.R.; Ribeiro, J.A.; Sebastião, A.M. Nitric oxide mediates interactions between GABAA receptors and adenosine A1 receptors in the rat hippocampus. Eur. J. Pharmacol., 2006, 543(1-3), 32-39.
83. Jeong, H.J.; Jang, I.S.; Nabekura, J.; Akaike, N. Adenosine A1 receptor-mediated presynaptic inhibition of GABAergic transmission in immature rat hippocampal CA1 neurons. J. Neurophysiol., 2003, 89(3), 1214-1222.
84. Lambert, N.A.; Teyler, T.J. Adenosine depresses excitatory but not fast inhibitory synaptic transmission in area CA1 of the rat hippocampus. Neurosci. Lett., 1991, 122(1), 50-52.
85. Li, H.; Henry, J.L. Adenosine action on interneurons and synaptic transmission onto interneurons in rat hippocampus in vitro. Eur. J. Pharmacol., 2000, 407(3), 237-244.
86. Yoon, K.W.; Rothman, S.M. Adenosine inhibits excitatory but not inhibitory synaptic transmission in the hippocampus. J. Neurosci., 1991, 11(5), 1375-1380.
87. Ochiishi, T.; Chen, L.; Yukawa, A.; Saitoh, Y.; Sekino, Y.; Arai, T.; Nakata, H.; Miyamoto, H. Cellular localization of adenosine A1 receptors in rat forebrain: immunohistochemical analysis using adenosine A1 receptor-specific monoclonal antibody. J. Comp. Neurol., 1999, 411(2), 301-316.
88. Cunha-Reis, D.; Ribeiro, J.A.; Sebastião, A.M. A1 and A2A receptor activation by endogenous adenosine is required for VIP enhancement of K+-evoked [3H]-GABA release from rat hippocampal nerve terminals. Neurosci. Lett., 2008, 430(3), 207-212.
89. Sousa, V.C.; Assaife-Lopes, N.; Ribeiro, J.A.; Pratt, J.A.; Brett, R.R.; Sebastião, A.M. Regulation of hippocampal cannabinoid CB1 receptor actions by adenosine A1 receptors and chronic caffeine administration: implications for the effects of Delta9-tetrahydrocannabinol on spatial memory. Neuropsychopharmacology, 2011, 36(2), 472-487.
90. Cristóvão-Ferreira, S.; Navarro, G.; Brugarolas, M.; Pérez-Capote, K.; Vaz, S.H.; Fattorini, G.; Conti, F.; Lluis, C.; Ribeiro, J.A.; McCormick, P.J.; Casadó, V.; Franco, R.; Sebastião, A.M. Modulation of GABA transport by adenosine A1R-A2AR heteromers, which are coupled to both Gs-and G(i/o)-proteins. J. Neurosci., 2011, 31(44), 15629-15639.
91. Cunha, R.A.; Milusheva, E.; Vizi, E.S.; Ribeiro, J.A.; Sebastião, A.M. Excitatory and inhibitory effects of A1 and A2A adenosine receptor activation on the electrically evoked [3H]acetylcholine release from different areas of the rat hippocampus. J. Neurochem., 1994, 63(1), 207-214.
92. Cunha, R.A.; Sebastião, A.M.; Ribeiro, J.A. Ecto-5'-nucleotidase is associated with cholinergic nerve terminals in the hippocampus but not in the cerebral cortex of the rat. J. Neurochem., 1992, 59(2), 657-666.
93. Goncalves, M.L.; Cunha, R.A.; Ribeiro, J.A. Adenosine A2A receptors facilitate 45Ca2+ uptake through class A calcium channels in rat hippocampal CA3 but not CA1 synaptosomes. Neurosci. Lett., 1997, 238(1-2), 73-77.
94. Bouron, A.; Reuter, H. Muscarinic stimulation of synaptic activity by protein kinase C is inhibited by adenosine in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA, 1997, 94(22), 12224-12229.
95. Delicado, E.G.; Rodrigues, A.; Sen, R.P.; Sebastião, A.M.; Ribeiro, J.A.; Miras-Portugal, M.T. Effect of 5'-(Nethylcarboxamido) adenosine on adenosine transport in cultured chromaffin cells. J. Neurochem., 1990, 54(6), 1941-1946.
96. Boulanger, L.M.; Poo, M.M. Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation. Nat. Neurosci., 1999, 2(4), 346-351.
97. Boulanger, L.; Poo, M.M. Gating of BDNF-induced synaptic potentiation by cAMP. Science, 1999, 284(5422), 1982-1984.
98. Lee, F.S.; Chao, M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. USA, 2001, 98(6), 3555-3560.
99. Tebano, M.T.; Martire, A.; Potenza, R.L.; Grò, C.; Pepponi, R.; Armida, M.; Domenici, M.R.; Schwarzschild, M.A.; Chen, J.F.; Popoli, P. Adenosine A(2A) receptors are required for normal BDNF levels and BDNF-induced potentiation of synaptic transmission in the mouse hippocampus. J. Neurochem., 2008, 104(1), 279-286.
100. Gomes, C.A.; Vaz, S.H.; Ribeiro, J.A.; Sebastião, A.M. Glial cell line-derived neurotrophic factor (GDNF) enhances dopamine release from striatal nerve endings in an adenosine A2A receptordependent manner. Brain Res., 2006, 1113(1), 129-136.
101. Pousinha, P.A.; Diógenes, M.J.; Ribeiro, J.A.; Sebastião, A.M. Triggering of BDNF facilitatory action on neuromuscular transmission by adenosine A2A receptors. Neurosci. Lett., 2006, 404(1-2), 143-147.
102. Assaife-Lopes, N.; Sousa, V.C.; Pereira, D.B.; Ribeiro, J.A.; Chao, M.V.; Sebastião, A.M. Activation of adenosine A2A receptors induces TrkB translocation and increases BDNF-mediated phospho-TrkB localization in lipid rafts: implications for neuromodulation. J. Neurosci., 2010, 30(25), 8468-8480.
103. Sebastião, A.M.; Assaife-Lopes, N.; Diógenes, M.J.; Vaz, S.H.; Ribeiro, J.A. Modulation of brain-derived neurotrophic factor (BDNF) actions in the nervous system by adenosine A(2A) receptors and the role of lipid rafts. Biochim. Biophys. Acta, 2011, 1808(5), 1340-1349.
104. Fernandes, C.C.; Pinto-Duarte, A.; Ribeiro, J.A.; Sebastião, A.M. Postsynaptic action of brain-derived neurotrophic factor attenuates alpha7 nicotinic acetylcholine receptor-mediated responses in hippocampal interneurons. J. Neurosci., 2008, 28(21), 5611-5618.
105. Vaz, S.H.; Cristóvão-Ferreira, S.; Ribeiro, J.A.; Sebastião, A.M. Brain-derived neurotrophic factor inhibits GABA uptake by the rat hippocampal nerve terminals. Brain Res., 2008, 1219, 19-25.
106. Vaz, S.H.; Jorgensen, T.N.; Cristóvão-Ferreira, S.; Duflot, S.; Ribeiro, J.A.; Gether, U.; Sebastião, A.M. 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., 2011, 286(47), 40464-40476.
107. Ferreira, J.M.; Paes-de-Carvalho, R. Long-term activation of adenosine A(2a) receptors blocks glutamate excitotoxicity in cultures of avian retinal neurons. Brain Res., 2001, 900(2), 169-176.
108. Wiese, S.; Jablonka, S.; Holtmann, B.; Orel, N.; Rajagopal, R.; Chao, M.V.; Sendtner, M. Adenosine receptor A2A-R contributes to motoneuron survival by transactivating the tyrosine kinase receptor TrkB. Proc. Natl. Acad. Sci. USA, 2007, 104(43), 17210-17215.
109. Golder, F.J.; Ranganathan, L.; Satriotomo, I.; Hoffman, M.; Lovett-Barr, M.R.; Watters, J.J.; Baker-Herman, T.L.; Mitchell, G.S. Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J. Neurosci., 2008, 28(9), 2033-2042.
110. Mojsilovic-Petrovic, J.; Jeong, G.B.; Crocker, A.; Arneja, A.; David, S.; Russell, D.S.; Kalb, R.G. Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors. J. Neurosci., 2006, 26(36), 9250-9263.
111. Katoh-Semba, R.; Kaneko, R.; Kitajima, S.; Tsuzuki, M.; Ichisaka, S.; Hata, Y.; Yamada, H.; Miyazaki, N.; Takahashi, Y.; Kato, K. Activation of p38 mitogen-activated protein kinase is required for in vivo brain-derived neurotrophic factor production in the rat hippocampus. Neuroscience, 2009, 163(1), 352-361.
112. Heese, K.; Fiebich, B.L.; Bauer, J.; Otten, U. Nerve growth factor (NGF) expression in rat microglia is induced by adenosine A2areceptors. Neurosci. Lett., 1997, 231(2), 83-86.
113. Ciccarelli, R.; Di Iorio, P.; Bruno, V.; Battaglia, G.; D'Alimonte, I.; D'Onofrio, M.; Nicoletti, F.; Caciagli, F. Activation of A(1) adenosine or mGlu3 metabotropic glutamate receptors enhances the release of nerve growth factor and S-100beta protein from cultured astrocytes. Glia, 1999, 27(3), 275-281.
114. Sebastião, A.M.; Macedo, M.P.; Ribeiro, J.A. Tonic activation of A(2A) adenosine receptors unmasks, and of A(1) receptors prevents, a facilitatory action of calcitonin gene-related peptide in the rat hippocampus. Br. J. Pharmacol., 2000, 129(2), 374-380.
115. Correia-de-Sá, P.; Timoteo, M.A.; Ribeiro, J.A. Synergism between A(2A)-adenosine receptor activation and vasoactive intestinal peptide to facilitate [3H]-acetylcholine release from the rat motor nerve terminals. Neurosci. Lett., 2001, 309(2), 101-104.
116. Cunha-Reis, D.; Sebastião, A.M.; Wirkner, K.; Illes, P.; Ribeiro, J.A. VIP enhances both pre-and postsynaptic GABAergic transmission to hippocampal interneurones leading to increased excitatory synaptic transmission to CA1 pyramidal cells. Br. J. Pharmacol., 2004, 143(6), 733-744.
117. Cunha-Reis, D.; Ribeiro, J.A.; Sebastião, A.M. VIP enhances synaptic transmission to hippocampal CA1 pyramidal cells through activation of both VPAC1 and VPAC2 receptors. Brain Res., 2005, 1049(1), 52-60.
118. Cunha-Reis, D.; Fontinha, B.M.; Ribeiro, J.A.; Sebastião, A.M. Tonic adenosine A1 and A2A receptor activation is required for the excitatory action of VIP on synaptic transmission in the CA1 area of the hippocampus. Neuropharmacology, 2007, 52(2), 313-320.
119. Serpa, A.; Ribeiro, J.A.; Sebastião, A.M. Cannabinoid CB(1) and adenosine A(1) receptors independently inhibit hippocampal synaptic transmission. Eur. J. Pharmacol., 2009, 623(1-3), 41-46.
120. Hoffman, A.F.; Laaris, N.; Kawamura, M.; Masino, S.A.; Lupica, C.R. Control of cannabinoid CB1 receptor function on glutamate axon terminals by endogenous adenosine acting at A1 receptors. J. Neurosci., 2010, 30(2), 545-555.
121. Kouznetsova, M.; Kelley, B.; Shen, M.; Thayer, S.A. Desensitization of cannabinoid-mediated presynaptic inhibition of neurotransmission between rat hippocampal neurons in culture. Mol. Pharmacol., 2002, 61(3), 477-485.
122. Straiker, A.J.; Borden, C.R.; Sullivan, J.M. G-protein alpha subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J. Neurosci., 2002, 22(7), 2460-2468.
123. Hájos, N.; Katona, I.; Naiem, S.S.; MacKie, K.; Ledent, C.; Mody, I.; Freund, T.F. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci., 2000, 12(9), 3239-3249.
124. Katona, I.; Sperlagh, B.; Sik, A.; Kafalvi, A.; Vizi, E.S.; Mackie, K.; Freund, T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci., 1999, 19(11), 4544-4558.
125. Freund, T.F.; Katona, I. Perisomatic inhibition. Neuron, 2007, 56(1), 33-42.
126. Wise, L.E.; Thorpe, A.J.; Lichtman, A.H. Hippocampal CB(1) receptors mediate the memory impairing effects of Delta(9)-tetrahydrocannabinol. Neuropsychopharmacology, 2009, 34(9), 2072-2080.
127. Puighermanal, E.; Marsicano, G.; Busquets-Garcia, A.; Lutz, B.; Maldonado, R.; Ozaita, A. Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci., 2009, 12(9), 1152-1158.
128. Snel, J.; Lorist, M.M. Effects of caffeine on sleep and cognition. Prog. Brain Res., 2011, 190, 105-117.
129. Koppelstaetter, F.; Poeppel, T.D.; Siedentopf, C.M.; Ischebeck, A.; Kolbitsch, C.; Mottaghy, F.M.; Felber, S.R.; Jaschke, W.R.; Krause, B.J. Caffeine and cognition in functional magnetic resonance imaging. J. Alzheimers Dis., 2010, 20(Suppl 1), S71-S84.
130. Ribeiro, J.A.; Sebastião, A.M. Caffeine and adenosine. J. Alzheimers Dis., 2010, 20(Suppl 1), S3-S15.
131. Varvel, S.A.; Anum, E.; Niyuhire, F.; Wise, L.E.; Lichtman, A.H. Delta(9)-THC-induced cognitive deficits in mice are reversed by the GABA(A) antagonist bicuculline. Psychopharmacology (Berl.), 2005, 178(2-3), 317-327.
132. Panlilio, L.V.; Ferré, S.; Yasar, S.; Thorndike, E.B.; Schindler, C.W.; Goldberg, S.R. Combined effects of THC and caffeine on working memory in rats. Br. J. Pharmacol., 2012, 165(8), 2529-2538.
133. Consroe, P.; Jones, B.; Laird, H., 2nd. EEG and behavioral effects of delta9-tetrahydrocannabinol in combination with stimulant drugs in rabbits. Psychopharmacology (Berl.), 1976, 50(1), 47-52.
134. Pedata, A.M.; Pugliese, A.M.; Sebastião, A.M.; Ribeiro, J.A. Adenosine A3 receptor signalling in the central nervous system, in: adenosine a3 receptors from cell biology to pharmacology and therapeutics; Borea, P.A., Ed.; Springer: London, 2010; pp. 165-188.
135. Biber, K.; Pinto-Duarte, A.; Wittendorp, M.C.; Dolga, A.M.; Fernandes, C.C.; Von Frijtag Drabbe Kunzel, J.; Keijser, J.N.; de Vries, R.; Ijzerman, A.P.; Ribeiro, J.A.; Eisel, U.; Sebastião, A.M.; Boddeke, H.W. Interleukin-6 upregulates neuronal adenosine A1 receptors: implications for neuromodulation and neuroprotection. Neuropsychopharmacology, 2008, 33(9), 2237-2250.
136. Moidunny, S.; Dias, R.B.; Wesseling, E.; Sekino, Y.; Boddeke, H.W.; Sebastião, A.M.; Biber, K. Interleukin-6-type cytokines in neuroprotection and neuromodulation: oncostatin M, but not leukemia inhibitory factor, requires neuronal adenosine A1 receptor function. J. Neurochem., 2010, 114(6), 1667-1677.
137. Almeida, C.G.; de Mendonça, A.; Cunha, R.A.; Ribeiro, J.A. Adenosine promotes neuronal recovery from reactive oxygen species induced lesion in rat hippocampal slices. Neurosci. Lett., 2003, 339(2), 127-130.