Astrocyte-originated ATP protects Aβ 1-42-induced impairment of synaptic plasticity

Journal of Neuroscience

Volumn 32, Issue 9, 2012, Pages 3081-3087

  Jung, Eun Sun ^a   An, Kyongman ^b   Hong, Hyun Seok ^c   Kim, Joung Hun ^b   Mook Jung, Inhee ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

^c Medifron DBT   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN [1-42]; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; POSTSYNAPTIC DENSITY PROTEIN 95; PURINERGIC P2 RECEPTOR; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL LINE, TUMOR; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; HUMANS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; NEURONAL PLASTICITY; PEPTIDE FRAGMENTS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84863282118     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6357-11.2012     Document Type: Article

References (65)

1. Abramov AY, Canevari L, Duchen MR (2003) Changes in intracellular calcium and glutathione in astrocytes as the primary mechanism of amyloid neurotoxicity. J Neurosci 23:5088-5095
2. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421
3. Angulo MC, Kozlov AS, Charpak S, Audinat E (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24:6920-6927
4. Araque A (2008) Astrocytes process synaptic information. Neuron Glia Biol 4:3-10
5. Béïque JC, Andrade R (2003) PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J Physiol 546:859-867
6. Benavides A, Pastor D, Santos P, Tranque P, Calvo S (2005) CHOP plays a pivotal role in the astrocyte death induced by oxygen and glucose deprivation. Glia 52:261-275
7. Bogdanov Y, Rubino A, Burnstock G (1998) Characterisation of subtypes of the P2X and P2Y families of ATP receptors in the foetal human heart. Life Sci 62:697-703
8. Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606-8620
9. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serumfree medium combination. J Neurosci Res 35:567-576
10. Burnstock G (1997) The past, present and future of purine nucleotides as signalling molecules. Neuropharmacology 36:1127-1139
11. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31-304
12. Chen QS, Kagan BL, Hirakura Y, Xie CW (2000) Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J Neurosci Res 60:65-72
13. Chow SK, Yu D, Macdonald CL, Buibas M, Silva GA (2010) Amyloid betapeptide directly induces spontaneous calcium transients, delayed intercellular calcium waves and gliosis in rat cortical astrocytes. ASN Neuro 2:e00026.
14. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354-1362
15. Collin C, Miyaguchi K, Segal M (1997) Dendritic spine density and LTP induction in cultured hippocampal slices. J Neurophysiol 77:1614-1623
16. Collingridge GL, Kehl SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334:33-46
17. Cullen WK, Suh YH, Anwyl R, Rowan MJ (1997) Block of LTP in rat hippocampus in vivo by beta-amyloid precursor protein fragments. Neuroreport 8:3213-3217
18. Daré E, Schulte G, Karovic O, Hammarberg C, Fredholm BB (2007) Modulation of glial cell functions by adenosine receptors. Physiol Behav 92:15-20
19. Elgersma Y, Silva AJ (1999) Molecular mechanisms of synaptic plasticity and memory. Curr Opin Neurobiol 9:209-213
20. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43:729-743
21. Geinisman Y (2000) Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb Cortex 10:952-962
22. Geinisman Y, deToledo-Morrell L, Morrell F (1991) Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res 566:77-88
23. Gordon GR, Baimoukhametova DV, Hewitt SA, Rajapaksha WR, Fisher TE, Bains JS (2005) Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 8:1078-1086
24. Halassa MM, Fellin T, Haydon PG (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13:54-63
25. Hynd MR, Scott HL, Dodd PR (2004) Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem Int 45:583-595
26. Illes P, Alexandre Ribeiro J (2004) Molecular physiology of P2 receptors in the central nervous system. Eur J Pharmacol 483:5-17
27. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, Masu M (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268:2836-2843
28. Kanjhan R, Housley GD, Thorne PR, Christie DL, Palmer DJ, Luo L, Ryan AF (1996) Localization of ATP-gated ion channels in cerebellum using P2x2R subunit-specific antisera. Neuroreport 7:2665-2669
29. Kaster MP, Rosa AO, Rosso MM, Goulart EC, Santos AR, Rodrigues AL (2004) Adenosine administration produces an antidepressant-like effect in mice: evidence for the involvement of A1 and A2A receptors. Neurosci Lett 355:21-24
30. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165-174
31. Kimelberg HK, Cai Z, Rastogi P, Charniga CJ, Goderie S, Dave V, Jalonen TO (1997) Transmitter-induced calcium responses differ in astrocytes acutely isolated from rat brain and in culture. J Neurochem 68:1088-1098
32. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740
33. Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci U S A 103:10058-10063
34. Kuchibhotla KV, Lattarulo CR, Hyman BT, Bacskai BJ (2009) Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323:1211-1215
35. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95:6448-6453
36. Lambrecht G (2000) Agonists and antagonists acting at P2X receptors: selectivity profiles and functional implications. Naunyn Schmiedebergs Arch Pharmacol 362:340-350
37. Lambrecht G, Braun K, Damer M, Ganso M, Hildebrandt C, Ullmann H, Kassack MU, Nickel P (2002) Structure-activity relationships of suramin and pyridoxal-5'-phosphate derivatives as P2 receptor antagonists. Curr Pharm Des 8:2371-2399
38. Lazarowski ER, Boucher RC, Harden TK (2003) Mechanisms of release of nucleotides and integration of their action as P2X-and P2Y-receptor activating molecules. Mol Pharmacol 64:785-795
39. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902
40. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDSADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 34:939-944
41. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221
42. Moser MB, Trommald M, Andersen P (1994) An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci U S A 91:12673-12675
43. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci U S A 102:5606-5611
44. Nakanishi S (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258:597-603
45. Niethammer M, Kim E, Sheng M (1996) Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 16:2157-2163
46. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067
47. Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, Sáez PJ, Jiang JX, Naus CC, Sáez JC, Giaume C (2011) Amyloid beta-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 31:4962-4977
48. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH (2006) Glia-derived D-serine controlsNMDAreceptor activity and synaptic memory. Cell 125:775-784
49. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-747
50. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116
51. Raff MC, Abney ER, Cohen J, Lindsay R, Noble M (1983) Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci 3:1289-1300
52. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413-492
53. Robertson SJ, Ennion SJ, Evans RJ, Edwards FA (2001) Synaptic P2X receptors. Curr Opin Neurobiol 11:378-386
54. Rubio ME, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641-653
55. Selkoe DJ (2000) The origins of Alzheimer disease: a is for amyloid. JAMA 283:1615-1617
56. Stix B, Reiser G (1998) Beta-amyloid peptide 25-35 regulates basal and hormone-stimulated Ca2+levels in cultured rat astrocytes. Neurosci Lett 243:121-124
57. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539
58. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R (2004) Block of longterm potentiation by naturally secreted and synthetic amyloid betapeptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogenactivated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 24:3370-3378
59. Wegiel J, Wang KC, Tarnawski M, Lach B (2000) Microglia cells are the driving force in fibrillar plaque formation, whereas astrocytes are a leading factor in plague degradation. Acta Neuropathol 100:356-364
60. Wísniewski HM, Robe A, Zigman W, Silverman W (1989) Neuropathological diagnosis of Alzheimer disease. J Neuropathol Exp Neurol 48:606-609
61. Yang Y, Ge W, Chen Y, Zhang Z, Shen W, Wu C, Poo M, Duan S (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci U S A 100:15194-15199
62. Yankner BA (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16:921-932
63. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40:971-982
64. Zhao D, Watson JB, Xie CW (2004) Amyloid beta prevents activation of calcium/calmodulin-dependent protein kinase II and AMPA receptor phosphorylation during hippocampal long-term potentiation. J Neurophysiol 92:2853-2858
65. Zimmermann H (1994) Signalling via ATP in the nervous system. Trends Neurosci 17:420-426.