Activation of presynaptic P2X7-like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase

Journal of Neuroscience

Volumn 22, Issue 14, 2002, Pages 5938-5945

  Armstrong, John N ^a   Brust, Tyson B ^a   Lewis, Randall G ^a   MacVicar, Brian A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

ATP; Glutamate; Hippocampus; Plasticity; Purinergic receptor; Synaptic depression

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 3' O (4 BENZOYLBENZOYL)ADENOSINE TRIPHOSPHATE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATE; ANTIBODY; CATION CHANNEL; CIBACRON BLUE F3GA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN; PURINE P2 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SYNTAXIN; ADENOSINE; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; DRUG DERIVATIVE; ENZYME INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PURINE P2X7 RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MOSSY FIBER; NEUROTRANSMISSION; NONHUMAN; PLASTICITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; NERVE CELL PLASTICITY; PATCH CLAMP; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPTOSOME; WESTERN BLOTTING;

ADENOSINE; ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; ENZYME ACTIVATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MITOGEN-ACTIVATED PROTEIN KINASES; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 0037098856     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-14-05938.2002     Document Type: Article

References (61)

1. Baricordi OR, Melchiorri L, Adinolfi E, Falzoni S, Chiozzi P, Buell G, Di Virgilio F (1999) Increased proliferation rate of lymphoid cells transfected with the P2X(7) ATP receptor. J Biol Chem 274:33206-33208.
2. Bennett MK, Calakos N, Scheller RH (1992) Syntaxin: A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257:255-259.
3. Bolshakov VY, Carboni L, Cobb MH, Siegelbaum SA, Belardetti F (2000) Dual MAP kinase pathways mediate opposing forms of longterm plasticity at CA3-CA1 synapses. Nat Neurosci 3:1107-1112.
4. Castillo PE, Weisskopf MG, Nicoll RA (1994) The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12:261-269.
5. Chessell IP, Michel AD, Humphrey PP (1997) Properties of the poreforming P2X7 purinoceptor in mouse NTW8 microglial cells. Br J Pharmacol 121:1429-1437.
6. Cunha RA, Ribeiro JA (2000) ATP as a presynaptic modulator. Life Sci 68:119-137.
7. Cunha RA, Sebastiao 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. Denlinger LC, Fisette PL, Sommer JA, Watters JJ, Prabhu U, Dubyak GR, Proctor RA, Bertics PJ (2001) Cutting edge: The nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J Immunol 167:1871-1876.
9. Deuchars SA, Atkinson L, Brooke RE, Musa H, Milligan CJ, Batten TF, Buckley NJ, Parson SH, Deuchars J (2001) Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143-7152.
10. Di Virgilio F (1995) The P2Z purinoceptor: An intriguing role in immunity, inflammation and cell death. Immunol Today 16:524-528.
11. Di Virgilio F, Sanz JM, Chiozzi P, Falzoni S (1999) The P2Z/P2X7 receptor of microglial cells: A novel immunomodulatory receptor. Prog Brain Res 120:355-368.
12. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31-55.
13. Dunwiddie TV, Diao L, Proctor WR (1997) Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J Neurosci 17:7673-7682.
14. Edwards FA, Gibb AJ (1993) ATP - A fast neurotransmitter. FEBS Lett 325:86-89.
15. Edwards FA, Gibb AJ, Colquhoun D (1992) ATP receptor-mediated synaptic currents in the central nervous system. Nature 359:144-147.
16. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F (1996) Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 156:1531-1539.
17. Ferrari D, Wesselborg S, Bauer MKA, Schulze-Osthoff K (1997) Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J Cell Biol 139:1635-1643.
18. Fitzjohn SM, Palmer MJ, May JE, Neeson A, Morris SA, Collingridge GL (2001) A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J Physiol (Lond) 537:421-430.
19. Fu WM, Poo MM (1991) ATP potentiates spontaneous transmitter release at developing neuromuscular synapses. Neuron 6:837-843.
20. Gu JG, MacDermott AB (1997) Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389:749-753.
21. Hide I, Tanaka M, Inoue A, Nakajima K, Kohsaka S, Inoue K, Nakata Y (2000) Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 75:965-972.
22. Hu Y, Fisette PL, Denlinger LC, Guadarrama AG, Sommer JA, Proctor RA, Bertics PJ (1998) Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J Biol Chem 273:27170-27175.
23. Impey S, Obrietan K, Storm DR (1999) Making new connections: Role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 23:11-14.
24. Inoue K, Nakazawa K, Fujimori K, Watano T, Takanaka A (1992) Extracellular adenosine 5′-triphosphate-evoked glutamate release in cultured hippocampal neurons. Neurosci Lett 134:215-218.
25. Inoue K, Koizumi S, Nakazawa K (1995) Glutamate-evoked release of adenosine 5′-triphosphate causing an increase in intracellular calcium in hippocampal neurons. NeuroReport 6:437-440.
26. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
27. Jahr CE, Jessell TM (1983) ATP excites a subpopulation of rat dorsal horn neurones. Nature 304:730-733.
28. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165-174.
29. Kim M, Jiang LH, Wilson HL, North RA, Surprenant A (2001) Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J 20:6347-6358.
30. Kukley M, Barden JA, Steinhauser C, Jabs R (2001) Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36:11-21.
31. Kusner DJ, Adams J (2000) ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D. J Immunol 164:379-388.
32. Le KT, Villeneuve P, Ramjaun AR, McPherson PS, Beaudet A, Seguela P (1998) Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors. Neuroscience 83:177-190.
33. MacDermott AB, Role LW, Siegelbaum SA (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485.
34. Manzoni OJ, Castillo PE, Nicoll RA (1995) Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacology 34:965-971.
35. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
36. Maruyama M, Sudo T, Kasuya Y, Shiga T, Hu B, Osada H (2000) Immunolocalization of p38 MAP kinase in mouse brain. Brain Res 887:350-358.
37. Murgia M, Hanau S, Pizzo P, Rippa M, Di Virgilio F (1993) Oxidized ATP. An irreversible inhibitor of the macrophage purinergic P2Z receptor. J Biol Chem 268:8199-8203.
38. Mutini C, Falzoni S, Ferrari D, Chiozzi P, Morelli A, Baricordi OR, Collo G, Ricciardi-Castagnoli P, Di Virgilio F (1999) Mouse dendritic cells express the P2X7 purinergic receptor: Characterization and possible participation in antigen presentation. J Immunol 163:1958-1965.
39. Nelson S, Toth L, Sheth B, Sur M (1994) Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265:774-777.
40. North RA, Barnard EA (1997) Nucleotide receptors. Curr Opin Neurobiol 7:346-357.
41. North RA, Surprenant A (2000) Pharmacology of cloned P2X receptors. Annu Rev Pharmacol Toxicol 40:563-580.
42. Panenka W, Jijon H, Herx LM, Armstrong JN, Feighan D, Wei T, Yong VW, Ransohoff RM, MacVicar BA (2001) P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J Neurosci 21:7135-7142.
43. Regehr WG, Delaney KR, Tank DW (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14:523-537.
44. Rubio M, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641-653.
45. Ruiz-Montasell B, Aguado F, Majo G, Chapman ER, Canals JM, Marsal J, Blasi J (1996) Differential distribution of syntaxin isoforms 1A and 1B in the rat central nervous system. Eur J Neurosci 8:2544-2552.
46. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct shortterm plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93:13304-13309.
47. Schmitz D, Frerking M, Nicoll RA (2000) Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27:327-338.
48. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL, Martin DL (1996) Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373:593-618.
49. Sun XP, Stanley EF (1996) An ATP-activated, ligand-gated ion channel on a cholinergic presynaptic nerve terminal. Proc Natl Acad Sci USA 93:1859-1863.
50. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735-738.
51. Terrian DM, Johnston D, Claiborne BJ, Ansah-Yiadom R, Strittmatter WJ, Rea MA (1988) Glutamate and dynorphin release from a subcellular fraction enriched in hippocampal mossy fiber synaptosomes. Brain Res Bull 21:343-351.
52. Terrian DM, Hernandez PG, Rea MA, Peters RI (1989) ATP release, adenosine formation, and modulation of dynorphin and glutamic acid release by adenosine analogues in rat hippocampal mossy fiber synaptosomes. J Neurochem 53:1390-1399.
53. Thummler S, Dunwiddie TV (2000) Adenosine receptor antagonists induce persistent bursting in the rat hippocampal CA3 region via an NMDA receptor-dependent mechanism. J Neurophysiol 83:1787-1795.
54. Vereker E, O'Donnell E, Lynch MA (2000) The inhibitory effect of interleukin-1β on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J Neurosci 20:6811-6819.
55. Virginio C, MacKenzie A, North RA, Surprenant A (1999) Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J Physiol (Lond) 519:335-346.
56. Visentin S, Renzi M, Frank C, Greco A, Levi G (1999) Two different ionotropic receptors are activated by ATP in rat microglia. J Physiol (Lond) 519:723-736.
57. White TD (1977) Direct detection of depolarisation-induced release of ATP from a synaptosomal preparation. Nature 267:67-68.
58. White TD (1978) Release of ATP from a synaptosomal preparation by elevated extracellular K+ and by veratridine. J Neurochem 30:329-336.
59. Wieraszko A, Seyfried TN (1989) ATP-induced synaptic potentiation in hippocampal slices. Brain Res 491:356-359.
60. Wilk-Blaszczak MA, Stein B, Xu S, Barbosa MS, Cobb MH, Belardetti F (1998) The mitogen-activated protein kinase p38-2 is necessary for the inhibition of N-type calcium current by bradykinin. J Neurosci 18:112-118.
61. Xiang Z, Brown TH (1998) Complex synaptic current waveforms evoked in hippocampal pyramidal neurons by extracellular stimulation of dentate gyrus. J Neurophysiol 79:2475-2484.