Activation of receptors negatively coupled to adenylate cyclase is required for induction of long-term synaptic depression at Schaffer collateral-CA1 synapses

Journal of Neurobiology

Volumn 66, Issue 3, 2006, Pages 205-219

  Santschi, Linda A ^a   Zhang, Xiao Lei ^b   Stanton, Patric K ^b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Adenosine; CA1; Cyclic GMP; Hippocampus; Long term depression; Metabotropic glutamate receptors; PKA; Synaptic plasticity

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR AGONIST; ADENOSINE A1 RECEPTOR ANTAGONIST; ADENYLATE CYCLASE; ALPHA CYCLOPROPYL 4 PHOSPHONOPHENYLGLYCINE; ALPHA ETHYLGLUTAMIC ACID; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC GMP; CYCLOHEXYLADENOSINE; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR ANTAGONIST; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PHOSPHODIESTERASE V INHIBITOR; UNCLASSIFIED DRUG; ZAPRINAST;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; LONG TERM DEPRESSION; MALE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION;

ADENYLATE CYCLASE; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; ORGAN CULTURE TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ADENOSINE A1; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 32044432119     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/neu.20213     Document Type: Article

References (64)

1. Bortolotto ZA, Fitzjohn SM, Collingridge GL. 1999. Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 9:299-304.
2. Broome MR, Collingridge GL, Irving AJ. 1994. Activation of the NO-cGMP signalling pathway depresses hippocampal synaptic transmission through an adenosine receptor-dependent mechanism. Neuropharmacology 33:1511-1513.
3. Cartmell J, Curtis AR, Kemp JA, Kendall DA, Alexander SPH. 1993. Subtypes of metabotropic excitatory amino acid receptors distinguished by stereoisomers of the rigid glutamate analogue, 1-aminocyclopenatane-1,3-dicarboxylate. Neurosci Lett 153:107-110.
4. Cartmell J, Kemp JA, Alexander SPJ, Shinozaki H, Kendall DA. 1994. Modulation of cyclic AMP formation by putative metabotropic receptor agonists. Br J Pharmacol 111:364-369.
5. Cho K, Kemp N, Noel J, Aggleton JP, Brown MW, Bashir ZI. 2000. A new form of long-term depression in the perirhinal cortex. Nat Neurosci 3:150-156.
6. Costenla AR, De Mendonça A, Ribeiro JA. 1999. Adenosine modulates synaptic plasticity in hippocampal slices from aged rats. Brain Res 851:228-234.
7. Cunha RA, Sebastião AM, Ribeiro JA. 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.
8. De Mondonça A, Almeida T, Bashir ZI, Ribeiro JA. 1997. Endogenous adenosine attenuates long-term depression and depotentiation in the CA1 region of the rat hippocampus. Neuropharmacology 36:161-167.
9. De Mondonça A, Ribeiro JA. 1999. Adenosine and neuronal plasticity. Life Sciences 60:245-251.
10. 2+ current through a mechanism independent of cGMP-dependent protein kinase. Neuron 1:693-699.
11. Dudek SM, Bear MF. 1992. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
12. Dunwiddie TV, Diao L. 1994. Extracellular adenosine concentrations in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J Pharmacol Exp Ther 268:537-545.
13. Gabriel A, Klussmann FW, Igelmund P. 1998. Rapid temperature changes induce adenosine mediated depression of synaptic transmission in hippocampal slices from rats (non-hibernators) but not in slices from golden hamsters (hibernators). Neuroscience 86:67-77.
14. Gage AT, Reyes M, Stanton PK. 1997. Nitric oxide-guanylyl-cyclase- dependent and independent components of multiple forms of long-term synaptic depression. Hippocampus 7:286-295.
15. o protein associated with the secretory granules. J Biol Chem 273:16913-16920.
16. Goh JW, Pennefather PS. 1989. A pertussis toxin-sensitive G protein in hippocampal long-term potentiation. Science 244:980-982.
17. Grover LM, Yan C. 1999. The modulation of excitatory synaptic transmission by adenosine in area CA1 of the rat hippocampus is temperature dependent. Neurosci Lett 263:77-80.
18. Haydon PG, Trudeau LE. 1998. Regulatory roles for GTP-binding proteins in nerve terminals. Sem Neurosci 9:220-231.
19. Huang CC, Liang YC, Hsu KS. 1999. A role for extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses. J Neurosci 19:9728-9738.
20. Ikeda SR, Lovinger DM, McCool BA, Lewis DL. 1995. Heterologous expression of metabotropic glutamate receptors in adult rat sympathetic neurons: subtype-specific coupling to ion channels. Neuron 14:1029-1038.
21. Izumi Y, Zorumski CF. 1993. Nitric oxide and long-term synaptic depression in the rat hippocampus. NeuroReport 4:1131-1134.
22. Jane DE, Thomas NK, Tse HW, Watkins JC. 1996. Potent antagonists at the L-AP4- and (1S, 3S)-ACPD-sensitive presynaptic metabotropic glutamate receptors in the neonatal rat spinal cord. Neuropharmacology 35:1029-1035.
23. Kato K. 1999. Adenosine as a neurotransmitter for the induction of long-term depression in rat CA1 pyramidal neurons. Soc Neurosci Abst 25:468.
24. Kemp M, Roberts P, Pook P, Jane D, Jones A, Jones P, Sunter D, et al. 1994. Antagonism of presynaptically mediated depressant responses and cyclic AMP-coupled metabotropic glutamate receptors. Eur J Pharm Mol Pharm Sec 266:187-192.
25. Kemp N, Bashir ZI. 1997. A role for adenosine in the regulation of long-term depression in the adult rat hippocampus in vitro. Neurosci Lett 225:189-192.
26. Lin HC, Wang SJ, Luo MZ, Gean PW. 2000. Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J Neurosci 20:9017-9024.
27. Lu KT, Gean PW. 1999. Masking of forskolin-induced long-term potentiation by adenosine accumulation in area CA1 of the rat hippocampus. Neurosci 88:69-78.
28. Manahan-Vaughan D. 1997. Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci 17:3303-3311.
29. Manahan-Vaughan D. 2000. Group III metabotropic glutamate receptors modulate long-term depression in the hippocampal CA1 region of two rat strains in vivo. Neuropharmacology 39:1952-1958.
30. Manganiello VC, Murata T, Taira M, Beifrage P, Degerman E. 1995. Diversity in cyclic nucleotide phosphodiesterase isoenzyme families. Archiv Biochem Biophys 322:1-13.
31. McCool BA, Pin JP, Brust PF, Harpold MM, Lovinger DM. 1996. Heterologous expression of rat group II metabotropic glutamate receptors (mGluR 2 and 3) in HEK 293 cells: functional coupling to a stably expressed conotoxin GVIA-sensitive calcium channel. Mol Pharmacol 50:912-922.
32. Mitchell JB, Lupica CR, Dunwiddie TV. 1993. Activity-dependent release of endogenous adenosine modulates synaptic responses in the rat hippocampus. J Neurosci 13:3439-3447.
33. Mons N, Harry A, Dubourg PP, Premont RT, Iyengar R, Cooper DMF. 1995. Immunohistochemical localization of adenylyl cyclase in rat brain indicated by highly selective concentration at synapses. Proc Natl Acad Sci USA 92:8473-8477.
34. Musgrave MA, Madigan MA, Bennett BM, Goh JW. 1994. Stimulation of postsynaptic and inhibition of presynaptic adenylyl cyclase activity by metabotropic glutamate receptor activation. J Neurochem 62:2316-2324.
35. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S. 1993. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11, 868-11,873.
36. Nakanishi S. 1994. Metabotropic glutamate receptor: Synaptic transmission modulation and plasticity. Neuron 13:1031-1037.
37. Neki A, Ohishi H, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. 1996. Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: an immunohistochemical study with a monoclonal antibody. Neurosci Lett 202:197-200.
38. Okamoto N, Hori S, Akazawa C, Hayashi Y, Shigemoto R, Mizuno N, Nakanishi S. 1994. Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J Biol Chem 269:1231-1236.
39. s-stimulated adenylyl cyclases. Curr Opin Neurobiol 3:345-351.
40. Pin JP, Duvoisin R. 1995. Review: Neurotransmitter receptors I. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
41. Qian J, Saggau P. 1999. Activity-dependent modulation of K+ currents at presynaptic terminals of mammalian central synapses. J Physiol 519:427-437.
42. Regehr WG, Tank DW. 1991. Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J Neurosci Meth 37:111-119.
43. Reyes-Harde M, Empson F, Potter BVL, Galione A, Stanton PK. 1999a. Evidence of a role for cyclic ADP-ribose in long-term synaptic depression in hippocampus. Proc Natl Acad Sci USA 96:4061-4066.
44. 2+ release from cyclic ADP ribose-sensitive stores. J Neurophysiol 82:1569-1576.
45. Santschi LA, Reyes-Harde M, Stanton PK. 1999. Chemically-induced, activity-independent LTD elicited by simultaneous activation of PKG and inhibition of PKA. J Neurophysiol 82:1577-1589.
46. Saugstad JA, Kinzie JM, Mulvihill ER, Segerson TP, Westbrook GL. 1994. Cloning and expression of a new member of the L-2-amino-4-phophonobutyric acid-class of metabotropic glutamate receptors. Mol Pharm 45:367-372.
47. Schoepp DD, Johnson BG. 1993. Pharmacology of metabotropic glutamate receptor inhibition of cyclic AMP formation in the adult rat hippocampus. Neurochem Int 3:277-283.
48. Shigemoto R, Kulik A, Roberts JDB, Ohishi H, Nusser Z, Kaneko T, Somogyi P. 1996. Target-cell specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature (London) 381:523-525.
49. Stanton PK, Chattarji S, Sejnowski TJ. 1991. 2-Amino-3-phosphonopropionic acid, an inhibitor of glutamate-stimulated phosphoinositide turnover, blocks induction of homosynaptic long-term depression, but not potentiation, in rat hippocampus. Neurosci Lett 127:61-66.
50. Stanton PK, Heinemann U, Müller W. 2001. FM1-43 imaging reveals cGMP-dependent long-term depression of presynaptic transmitter release. J Neurosci 21:RC167 (1-6).
51. Stanton PK, Winterer J, Bailey CP, Kyrozis A, Raginov I, Laube G, Veh RW, et al. 2003. Long-term depression of presynaptic release from the readily-releasable vesicle pool induced by NMDA receptor-dependent retrograde nitric oxide. J Neurosci 23:5936-5944.
52. Swanson TH, Drazba JA, Rivkees SA. 1996. Adenosine A1 receptors are located predominantly on axons in the rat hippocampal formation. J Comp Neurol 363:517-531.
53. Takumi Y, Bergersen L, Landsend AS, Rinvik E, Ottersen OP. 1998. Synaptic arrangement of glutamate receptors. Prog Brain Res 116:105-121.
54. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S. 1992. A family of metabotropic glutamate receptors. Neuron 8:169-179.
55. Tanabe Y, Nomura A, Masu M, Shigemoto R, Mizuno N, Nakanishi S. 1993. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13:1372-1378.
56. Thomsen C, Kristensen P, Mulvihill E, Haldeman B, Suzdak PD. 1992. L-2-amino-4-phosphonobutyrate (L-AP4) is an agonist at the type IV metabotropic glutamate receptor which is negatively coupled to adenylate cyclase. Eur J Pharm 227:361-362.
57. Toms NJ, Jane DE, Kemp MC, Bedingfield JS, Roberts PJ. 1996. The effects of (RS)-alpha-cyclopropyl-4-phosphonophenylglycine ((RS)-CPPG), a potent and selective metabotropic glutamate receptor antagonist. Br J Pharm 119:851-854.
58. Westenbroek RE, Hell JW, Warner C, Duber SJ, Snutch TB, Catterall WA. 1992. Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. Neuron 9:1099-1115.
59. Wu LW, Saggau P. 1994a. Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12:1139-1148.
60. Wu LW, Saggau P. 1994b. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of the hippocampus. J Neurosci 14:645-654.
61. Wu LW, Saggau P. 1994c. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J Neurosci 14:5613-5622.
62. 2+ influx. J Physiol 485:649-657.
63. Xiao MY, Niu YP, Wigstrom H. 1997. Comparing long-term depression with pharmacologically induced synaptic attenuations in young rat hippocampi. Synapse 26:329-340.
64. Zhang C, Schmidt JT. 1999. Adenosine A1 and class II metabotropic glutamate receptors mediate shared presynaptic inhibition of retinotectal transmission. J Neurophysiol 82:2947-2955.