The expression of kainate receptor subunits in hippocampal astrocytes after experimentally induced status epilepticus

Journal of Neuropathology and Experimental Neurology

Volumn 72, Issue 10, 2013, Pages 919-932

  Vargas, Jay R ^a   Takahashi, D Koji ^b   Thomson, Kyle E ^c   Wilcox, Karen S ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c University of Utah   (United States)

Author keywords

Astrogliosis; Epilepsy; Glutamate receptor; Kainic acid

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; GLUTAMATE RECEPTOR 5; KAINIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN CORTEX; BRAIN STEM; CELL LOSS; CONTROLLED STUDY; CORPUS STRIATUM; EPILEPTIC STATE; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ASTROCYTES; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HIPPOCAMPUS; KAINIC ACID; MALE; NEURONS; PILOCARPINE; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; SEIZURES; STATUS EPILEPTICUS;

EID: 84885029060     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182a4b266     Document Type: Article

References (61)

1. Engel J Jr. Clinical evidence for the progressive nature of epilepsy. Epilepsy Res Suppl 1996;12:9-20
2. Kanner AM. Mood disorder and epilepsy: A neurobiologic perspective of their relationship. Dialogues Clin Neurosci 2008;10:39-45 (Pubitemid 351542977)
3. Mohanraj R, Brodie MJ. Diagnosing refractory epilepsy: Response to sequential treatment schedules. Eur J Neurol 2006;13:277-82
4. Binder DK, Steinhauser C. Functional changes in astroglial cells in epilepsy. Glia 2006;54:358-68 (Pubitemid 44422938)
5. Oberheim NA, Tian GF, Han X, et al. Loss of astrocytic domain organization in the epileptic brain. J Neurosci 2008;28:3264-76 (Pubitemid 351469330)
6. de Lanerolle NC, Lee TS, Spencer DD. Astrocytes and epilepsy. Neurotherapeutics 2010;7:424-38
7. Spencer SS, Kim J, deLanerolle N, et al. Differential neuronal and glial relations with parameters of ictal discharge in mesial temporal lobe epilepsy. Epilepsia 1999;40:708-12 (Pubitemid 29260708)
8. Beattie EC, Stellwagen D, Morishita W, et al. Control of synaptic strength by glial TNFalpha. Science 2002;295:2282-85 (Pubitemid 34258846)
9. Stellwagen D, Malenka RC. Synaptic scaling mediated by glial TNF-alpha. Nature 2006;440:1054-59
10. Dingledine R. Glutamatergic mechanisms related to epilepsy: Ionotropic receptors. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper's Basic Mechanisms of the Epilepsies. Bethesda, MD: Oxford University Press;2012
11. Traynelis SF, Wollmuth LP, McBain CJ, et al. Glutamate receptor ion channels: Structure, regulation, and function. Pharmacol Rev 2010;62: 405-96
12. Jabs R, Kirchhoff F, Kettenmann H, et al. Kainate activates Ca(2+)-permeable glutamate receptors and blocks voltage-gated K+ currents in glial cells of mouse hippocampal slices. Pflugers Arch 1994;426:310-19
13. Porter JT, McCarthy KD. GFAP-positive hippocampal astrocytes in situ respond to glutamatergic neuroligands with increases in [Ca2+]i. Glia 1995;13:101-12
14. Steinhauser C, Jabs R, Kettenmann H. Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice. Hippocampus 1994;4:19-35 (Pubitemid 24168377)
15. Bergles DE, Jabs R, Steinhauser C. Neuron-glia synapses in the brain. Brain Res Rev 2010;63:130-37
16. Cahoy JD, Emery B, Kaushal A, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 2008;28:264-78
17. Condorelli DF, Dell'Albani P, Amico C, et al. Induction of primary response genes by excitatory amino acid receptor agonists in primary astroglial cultures. J Neurochem 1993;60:877-85 (Pubitemid 23066705)
18. Gottlieb M, Matute C. Expression of ionotropic glutamate receptor subunits in glial cells of the hippocampal CA1 area following transient forebrain ischemia. J Cereb Blood Flow Metab 1997;17:290-300 (Pubitemid 27161372)
19. Krebs C, Fernandes HB, Sheldon C, et al. Functional NMDA receptor subtype 2B is expressed in astrocytes after ischemia in vivo and anoxia in vitro. J Neurosci 2003;23:3364-72 (Pubitemid 36531978)
20. Lerma J, Paternain AV, Rodriguez-Moreno A, et al. Molecular physiology of kainate receptors. Physiol Rev 2001;81:971-98 (Pubitemid 32611226)
21. Rodriguez-Moreno A, Sihra TS. Kainate receptors with a metabotropic modus operandi. Trends Neurosci 2007;30:630-37 (Pubitemid 350101852)
22. Rozas JL, Paternain AV, Lerma J. Noncanonical signaling by ionotropic kainate receptors. Neuron 2003;39:543-53 (Pubitemid 36937053)
23. Seifert G, Carmignoto G, Steinhauser C. Astrocyte dysfunction in epilepsy. Brain Res Rev 2010;63:212-21
24. Takahashi DK, Vargas JR, Wilcox KS. Increased coupling and altered glutamate transport currents in astrocytes following kainic acidYinduced status epilepticus. Neurobiol Dis 2010;40:573-85
25. Hellier JL, Patrylo PR, Buckmaster PS, et al. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: Assessment of a rat model of temporal lobe epilepsy. Epilepsy Res 1998; 31:73-84 (Pubitemid 28305406)
26. Smith MD, Adams AC, Saunders GW, et al. Phenytoin-and carbamazepine-resistant spontaneous bursting in rat entorhinal cortex is blocked by retigabine in vitro. Epilepsy Res 2007;74:97-106 (Pubitemid 46654739)
27. Williams PA, White AM, Clark S, et al. Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci 2009;29:2103-12
28. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972;32:281-94
29. White HS, Alex AB, Pollock A, et al. A new derivative of valproic acid amide possesses a broad-spectrum antiseizure profile and unique activity against status epilepticus and organophosphate neuronal damage. Epilepsia 2012;53:134-46
30. Yoneyama M, Kitayama T, Taniura H, et al. Immersion fixation with Carnoy solution for conventional immunohistochemical detection of particular N-methyl-D-aspartate receptor subunits in murine hippocampus. J Neurosci Res 2003;73:416-26 (Pubitemid 36918105)
31. Eyigor O, Minbay Z, Cavusoglu I, et al. Localization of kainate receptor subunit GluR5-immunoreactive cells in the rat hypothalamus. Brain Res Mol Brain Res 2005;136:38-44 (Pubitemid 40704607)
32. Zack GW, Rogers WE, Latt SA. Automatic measurement of sister chromatid exchange frequency. J Histochem Cytochem 1977;25:741-53 (Pubitemid 8185325)
33. Dunkley PR, Jarvie PE, Robinson PJ. A rapid Percoll gradient procedure for preparation of synaptosomes. Nature protocols 2008;3:1718-28
34. Nakamura Y, Iga K, Shibata T, et al. Glial plasmalemmal vesicles: A subcellular fraction from rat hippocampal homogenate distinct from synaptosomes. Glia 1993;9:48-56
35. Nakamura Y, Kubo H, Kataoka K. Uptake of transmitter amino acids by glial plasmalemmal vesicles from different regions of rat central nervous system. Neurochem Res 1994;19:1145-50 (Pubitemid 24284789)
36. Stigliani S, Zappettini S, Raiteri L, et al. Glia re-sealed particles freshly prepared from adult rat brain are competent for exocytotic release of glutamate. J Neurochem 2006;96:656-68
37. Riddle EL, Topham MK, Haycock JW, et al. Differential trafficking of the vesicular monoamine transporter-2 by methamphetamine and cocaine. Eur J Pharmacol 2002;449:71-74
38. Ben-Ari Y, Cossart R. Kainate, a double agent that generates seizures: Two decades of progress. Trends in neurosciences 2000;23:580-87
39. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 1985;5: 1016-22 (Pubitemid 15123049)
40. Fernaud-Espinosa I, Nieto-Sampedro M, et al. Differential activation of microglia and astrocytes in aniso-and isomorphic gliotic tissue. Glia 1993;8:277-91
41. Kálmán M. Glia reaction and reactive glia. Adv Molec Cell Biol 2003;31: 787-835
42. Bernardinelli Y, Magistretti PJ, Chatton JY. Astrocytes generate Na+-mediated metabolic waves. Proc Natl Acad Sci U S A 2004;101: 14937-42 (Pubitemid 39410778)
43. Chatton JY, Pellerin L, Magistretti PJ. GABA uptake into astrocytes is not associated with significant metabolic cost: Implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci U S A 2003;100: 12456-61 (Pubitemid 37271581)
44. Pellerin L, Magistretti PJ. Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 1994;91:10625-29 (Pubitemid 24329051)
45. Bezzi P, Carmignoto G, Pasti L, et al. Prostaglandins stimulate calciumdependent glutamate release in astrocytes. Nature 1998;391:281-85 (Pubitemid 28099014)
46. Fellin T, Pascual O, Gobbo S, et al. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 2004;43:729-43 (Pubitemid 39179731)
47. Parpura V, Basarsky TA, Liu F, et al. Glutamate-mediated astrocyte-neuron signalling. Nature 1994;369:744-47 (Pubitemid 24225363)
48. Fellin T, Gomez-Gonzalo M, Gobbo S, et al. Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci 2006;26:9312-22 (Pubitemid 44359857)
49. Tian GF, Azmi H, Takano T, et al. An astrocytic basis of epilepsy. Nat Med 2005;11:973-81 (Pubitemid 41294443)
50. Cornell-Bell AH, Finkbeiner SM, Cooper MS, et al. Glutamate induces calcium waves in cultured astrocytes: Long-range glial signaling. Science 1990;247:470-73
51. Montana V, Malarkey EB, Verderio C, et al. Vesicular transmitter release from astrocytes. Glia 2006;54:700-15 (Pubitemid 44629633)
52. Porter JT, McCarthy KD. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 1996;16:5073-81 (Pubitemid 26269667)
53. Scemes E, Giaume C. Astrocyte calcium waves: What they are and what they do. Glia 2006;54:716-25 (Pubitemid 44629634)
54. Petravicz J, Fiacco TA, McCarthy KD. Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci 2008;28:4967-73
55. Lee SH, Magge S, Spencer DD, et al. Human epileptic astrocytes exhibit increased gap junction coupling. Glia 1995;15:195-202
56. Manning TJ Jr, Sontheimer H. Spontaneous intracellular calcium oscillations in cortical astrocytes from a patient with intractable childhood epilepsy (Rasmussen's encephalitis). Glia 1997;21:332-37 (Pubitemid 27491053)
57. Das A, Wallace GCt, Holmes C, et al. Hippocampal tissue of patients with refractory temporal lobe epilepsy is associated with astrocyte activation, inflammation, and altered expression of channels and receptors. Neuroscience 2012;220:237-46
58. Bahn S, Volk B, Wisden W. Kainate receptor gene expression in the developing rat brain. J Neurosci 1994;14:5525-47 (Pubitemid 24279070)
59. Ritter LM, Vazquez DM, Meador-Woodruff JH. Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res Dev Brain Res 2002;139:227-36 (Pubitemid 35453909)
60. Darstein M, Petralia RS, Swanson GT, et al. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 2003; 23:8013-19 (Pubitemid 37082453)
61. Fogarty DJ, Perez-Cerda F, Matute C. KA1-like kainate receptor subunit immunoreactivity in neurons and glia using a novel anti-peptide antibody. Brain Res Mol Brain Res 2000;81:164-76