Astrocyte control of synaptic NMDA receptors contributes to the progressive development of temporal lobe epilepsy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 43, 2013, Pages 17540-17545

  Clasadonte, Jerome ^a   Dong, Jinghui ^a   Hines, Dustin J ^a   Haydon, Philip G ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Electroencephalography; Glia to neuron signaling; Hippocampus; Interictal spikes; Pilocarpine mouse

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PILOCARPINE; SNARE PROTEIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BEHAVIOR DISORDER; BRAIN DAMAGE; CONTROLLED STUDY; DENTATE HILUS; DISEASE SEVERITY; EPILEPTIC STATE; EPILEPTOGENESIS; GENOTYPE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; MALE; MOLECULAR GENETICS; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY;

ELECTROENCEPHALOGRAPHY; GLIA-TO-NEURON SIGNALING; HIPPOCAMPUS; INTERICTAL SPIKES; PILOCARPINE MOUSE;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; ASTROCYTES; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; PILOCARPINE; RECEPTORS, N-METHYL-D-ASPARTATE; SNARE PROTEINS; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 84886434371     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311967110     Document Type: Article

References (31)

1. Kwan P, Schachter SC, Brodie MJ (2011) Drug-resistant epilepsy. N Engl J Med 365(10): 919-926.
2. Halassa MM, Haydon PG (2010) Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335-355.
3. Seifert G, Carmignoto G, Steinhäuser C (2010) Astrocyte dysfunction in epilepsy. Brain Res Brain Res Rev 63(1-2):212-221.
4. Clasadonte J, Haydon PG (2012) Astrocytes and epilepsy. Jasper's Basic Mechanisms of the Epilepsies, eds Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV (Oxford Univ Press, New York), 4th Ed, pp 591-605.
5. Fellin T, et al. (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci USA 106(35):15037-15042.
6. Deng Q, Terunuma M, Fellin T, Moss SJ, Haydon PG (2011) Astrocytic activation of A1 receptors regulates the surface expression of NMDA receptors through a Src kinase dependent pathway. Glia 59(7):1084-1093.
7. Ghasemi M, Schachter SC (2011) The NMDA receptor complex as a therapeutic target in epilepsy: A review. Epilepsy Behav 22(4):617-640.
8. Pascual O, et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113-116.
9. Curia G, Longo D, Biagini G, Jones RS, Avoli M (2008) The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172(2):143-157.
10. Gröticke I, Hoffmann K, Löscher W (2007) Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp Neurol 207(2):329-349.
11. White A, et al. (2010) EEG spike activity precedes epilepsy after kainate-induced status epilepticus. Epilepsia 51(3):371-383.
12. Goffin K, Nissinen J, Van Laere K, Pitkänen A (2007) Cyclicity of spontaneous recurrent seizures in pilocarpine model of temporal lobe epilepsy in rat. Exp Neurol 205(2):501-505.
13. Swinkels WA, Kuyk J, van Dyck R, Spinhoven P (2005) Psychiatric comorbidity in epilepsy. Epilepsy Behav 7(1):37-50.
14. Müller CJ, Gröticke I, Bankstahl M, Löscher W (2009) Behavioral and cognitive alterations, spontaneous seizures, and neuropathology developing after a pilocarpineinduced status epilepticus in C57BL/6 mice. Exp Neurol 219(1):284-297.
15. Borges K, et al. (2003) Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp Neurol 182(1):21-34.
16. Ortinski PI, et al. (2010) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13(5):584-591.
17. Williams PA, et al. (2009) Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci 29(7):2103-2112.
18. Kadam SD, White AM, Staley KJ, Dudek FE (2010) Continuous electroencephalographic monitoring with radio-telemetry in a rat model of perinatal hypoxia-ischemia reveals progressive post-stroke epilepsy. J Neurosci 30(1):404-415.
19. Engel J, Jr. (1996) Clinical evidence for the progressive nature of epilepsy. Epilepsy Res Suppl 12:9-20.
20. Haut SR (2006) Seizure clustering. Epilepsy Behav 8(1):50-55.
21. Gómez-Gonzalo M, et al. (2010) An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol 8(4):e1000352.
22. Sanna PP, et al. (2000) A role for Src kinase in spontaneous epileptiform activity in the CA3 region of the hippocampus. Proc Natl Acad Sci USA 97(15):8653-8657.
23. Kojima N, Ishibashi H, Obata K, Kandel ER (1998) Higher seizure susceptibility and enhanced tyrosine phosphorylation of N-methyl-D-aspartate receptor subunit 2B in fyn transgenic mice. Learn Mem 5(6):429-445.
24. Halassa MM, et al. (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61(2):213-219.
25. Schmitt LI, Sims RE, Dale N, Haydon PG (2012) Wakefulness affects synaptic and network activity by increasing extracellular astrocyte-derived adenosine. J Neurosci 32(13):4417-4425.
26. Tian GF, et al. (2005) An astrocytic basis of epilepsy. Nat Med 11(9):973-981.
27. Fellin T, Gomez-Gonzalo M, Gobbo S, Carmignoto G, Haydon PG (2006) Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci 26(36):9312-9322.
28. Mothet JP, et al. (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci USA 102(15):5606-5611.
29. Heinrich A, Andó RD, Túri G, Rózsa B, Sperlágh B (2012) K+ depolarization evokes ATP, adenosine and glutamate release from glia in rat hippocampus: A microelectrode biosensor study. Br J Pharmacol 167(5):1003-1020.
30. Shigetomi E, Jackson-Weaver O, Huckstepp RT, O'Dell TJ, Khakh BS (2013) TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J Neurosci 33(24):10143-10153.
31. Crawley JN (2008) Behavioral phenotyping strategies for mutant mice. Neuron 57(6): 809-818.