Loss of astrocytic domain organization in the epileptic brain

Journal of Neuroscience

Volumn 28, Issue 13, 2008, Pages 3264-3276

  Oberheim, Nancy Ann ^a,b   Tian, Guo Feng ^a   Han, Xiaoning ^a   Peng, Weiguo ^a   Takano, Takahiro ^a   Ransom, Bruce ^b   Nedergaard, Maiken ^a,c  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Dendritic sprouting; Diolistic labeling; EEG; Fluorescence microscopy; Glia; Mice model

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTICONVULSIVE AGENT; GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID; MUTANT PROTEIN; VALPROIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN INJURY; CELL LABELING; CONTROLLED STUDY; DENDRITE; EPILEPSY; GENETIC SUSCEPTIBILITY; GLIOSIS; MOUSE; NERVE CELL EXCITABILITY; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; TRANSGENIC MOUSE; UPREGULATION;

AMINO ACIDS; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTICONVULSANTS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BEHAVIOR, ANIMAL; BRAIN; DENDRITES; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; TIME FACTORS; VALPROIC ACID;

EID: 41549146380     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4980-07.2008     Document Type: Article

References (72)

1. Amatniek JC, Hauser WA, DelCastillo-Castaneda C, Jacobs DM, Marder K, Bell K, Albert M, Brandt J, Stern Y (2006) Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47:867-872.
2. Annegers JF, Hauser WA, Coan SP, Rocca WA (1998) A population-based study of seizures after traumatic brain injuries. N Engl J Med 338:20-24.
3. Ayala GX, Tapia R (2003) Expression of heat shock protein 70 induced by 4-aminopyridine through glutamate-mediated excitotoxic stress in rat hippocampus in vivo. Neuropharmacology 45:649-660.
4. Bausch SB, He S, Petrova Y, Wang XM, McNamara JO (2006) Plasticity of both excitatory and inhibitory synapses is associated with seizures induced by removal of chronic blockade of activity in cultured hippocampus. J Neurophysiol 96:2151-2167.
5. Ben-Ari Y, Cossart R (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23:580-587.
6. Benediktsson AM, Schachtele SJ, Green SH, Dailey ME (2005) Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures. J Neurosci Methods 141:41-53.
7. Bignami A, Dahl D (1976) The astroglial response to stabbing: immunofluorescence studies with antibodies to astrocyte-specific protein (GFA) in mammalian and submammalian vertebrates. Neuropathol Appl Neurobiol 2:99-111.
8. Bordey A, Sontheimer H (1998) Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 32:286-303.
9. Bragin A, Engel Jr J, Wilson CL, Vizentin E, Mathern GW (1999) Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia 40:1210-1221.
10. Brenner M, Johnson AB, Boespflug-Tanguy O, Rodriguez D, Goldman JE, Messing A (2001) Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat Genet 27:117-120.
11. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
12. Castiglioni AJ, Peterson SL, Sanabria EL, Tiffany-Castiglioni E (1990) Structural changes in astrocytes induced by seizures in a mode of temporal lobe epilepsy. J Neurosci Res 26:334-341.
13. Chen K, Baram TZ, Soltesz I (1999) Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits. Nat Med 5:888-894.
14. Chvatal A, Anderova M, Kirchhoff F (2007) Three-dimensional confocal morphometry - a new approach for studying dynamic changes in cell morphology in brain slices. J Anat 210:671-683.
15. Eid T, Thomas MJ, Spencer DD, Runden-Pran E, Lai JC, Malthankar GV, Kim JH, Danbolt NC, Ottersen OP, de Lanerolle NC (2004) Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363:28-37.
16. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjornsen LP, Spencer DD, Agre P, Ottersen OP, de Lanerolle NC (2005) Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci USA 102:1193-1198.
17. Frankel WN, Taylor BA, Noebels JL, Lutz CM (1994) Genetic epilepsy model derived from common inbred mouse strains. Genetics 138:481-489.
18. Frey LC (2003) Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 44 [Suppl 10]:11-17.
19. Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW (2000) Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 27:219-225.
20. Golarai G, Greenwood AC, Feeney DM, Connor JA (2001) Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J Neurosci 21:8523-8537.
21. Graham D, Lantos P (1997) Greenfields' neuropathology, Ed 6. London: Arnold.
22. Guerreiro MM, Quesney LF, Salanova V, Snipes GJ (2003) Continuous electrocorticogram epileptiform discharges due to brain gliosis. J Clin Neurophysiol 20:239-242.
23. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG (2007) Synaptic islands defined by the territory of a single astrocyte. J Neurosci 27:6473-6477.
24. Hammond EJ, Ramsay RE, Villarreal HJ, Wilder BJ (1980) Effects of intracortical injection of blood and blood components on the electrocorticogram. Epilepsia 21:3-14.
25. Hauser WA, Morris ML, Heston LL, Anderson VE (1986) Seizures and myoclonus in patients with Alzheimer's disease. Neurology 36:1226-1230.
26. Heinemann U, Gabriel S, Jauch R, Schulze K, Kivi A, Eilers A, Kovacs R, Lehmann TN (2000) Alterations of glial cell function in temporal lobe epilepsy. Epilepsia 41 [Suppl 6]:S185-S189.
27. Hellier JL, Patrylo PR, Buckmaster PS, Dudek FE (1998) Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res 31:73-84.
28. Hinterkeuser S, Schroder W, Hager G, Seifert G, Blumcke I, Elger CE, Schramm J, Steinhauser C (2000) Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 12:2087-2096.
29. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
30. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117-1124.
31. Kopniczky Z, Dobo E, Borbely S, Vilagi I, Detari L, Krisztin-Peva B, Bagosi A, Molnar E, Mihaly A (2005) Lateral entorhinal cortex lesions rearrange afferents, glutamate receptors, increase seizure latency and suppress seizure-induced c-fos expression in the hippocampus of adult rat. J Neurochem 95:111-124.
32. Lange SC, Neafsey EJ, Wyler AR (1980) Neuronal activity in chronic ferric chloride epileptic foci in cats and monkey. Epilepsia 21:251-254.
33. Leite JP, Garcia-Cairasco N, Cavalheiro EA (2002) New insights from the use of pilocarpine and kainate models. Epilepsy Res 50:93-103.
34. Leite JP, Neder L, Arisi GM, Carlotti Jr CG, Assirati JA, Moreira JE (2005) Plasticity, synaptic strength, and epilepsy: what can we learn from ultrastructural data? Epilepsia 46 [Suppl 5]:134-141.
35. Loscher W (2002) Basic pharmacology of valproate: a review after 35 years of clinical use for the treatment of epilepsy. CNS Drugs 16:669-694.
36. Maragakis NJ, Rothstein JD (2004) Glutamate transporters: animal models to neurologic disease. Neurobiol Dis 15:461-473.
37. Maragakis NJ, Rothstein JD (2006) Mechanisms of disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2:679-689.
38. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson N, Leite JP, Chimelli L, Born DE, Sakamoto AC, Assirati JA, Fried I, Peacock WJ, Ojemann GA, Adelson PD (1999) Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52:453-472.
39. McGraw J, Hiebert GW, Steeves JD (2001) Modulating astrogliosis after neurotrauma. J Neurosci Res 63:109-115.
40. McKhann II GM, Schoenfeld-McNeill J, Born DE, Haglund MM, Ojemann GA (2000) Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. J Neurosurg 93:44-52.
41. Mehlhorn G, Hollborn M, Schliebs R (2000) Induction of cytokines in glial cells surrounding cortical beta-amyloid plaques in transgenic Tg2576 mice with Alzheimer pathology. Int J Dev Neurosci 18:423-431.
42. Messori A, Polonara G, Carle F, Gesuita R, Salvolini U (2005) Predicting posttraumatic epilepsy with MRI: prospective longitudinal morphologic study in adults. Epilepsia 46:1472-1481.
43. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622.
44. Nishida H, Okabe S (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27:331-340.
45. Oberheim NA, Wang X, Goldman S, Nedergaard M (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547-553.
46. Ogata K, Kosaka T (2002) Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113:221-233.
47. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:697-711.
48. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, Schrama LH, van Veelen CW, van Rijen PC, van Nieuwenhuizen O, Gispen WH, de Graan PN (2002) Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125:32-43.
49. Reid SA, Sypert GW (1980) Acute FeCl3-induced epileptogenic foci in cats: electrophysiological analyses. Brain Res 188:531-542.
50. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38:73-84.
51. Samuelsson C, Kumlien E, Flink R, Lindholm D, Ronne-Engstrom E (2000) Decreased cortical levels of astrocytic glutamate transport protein GLT-1 in a rat model of posttraumatic epilepsy. Neurosci Lett 289:185-188.
52. Schauwecker PE (2003) Genetic basis of kainate-induced excitotoxicity in mice: phenotypic modulation of seizure-induced cell death. Epilepsy Res 55:201-210.
53. Schroder W, Hinterkeuser S, Seifert G, Schramm J, Jabs R, Wilkin GP, Steinhauser C (2000) Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia 41 [Suppl 6]:S181-S184.
54. Sinha S, Naritoku DK (2000) Intravenous valproate is well tolerated in unstable patients with status epilepticus. Neurology 55:722-724.
55. Suzuki F, Makiura Y, Guilhem D, Sorensen JC, Onteniente B (1997) Correlated axonal sprouting and dendritic spine formation during kainate-induced neuronal morphogenesis in the dentate gyrus of adult mice. Exp Neurol 145:203-213.
56. Swann JW, Al-Noori S, Jiang M, Lee CL (2000) Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10:617-625.
57. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
58. Tavazoie SF, Alvarez VA, Ridenour DA, Kwiatkowski DJ, Sabatini BL (2005) Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci 8:1727-1734.
59. Terai K, Iwai A, Kawabata S, Sasamata M, Miyata K, Yamaguchi T (2001) Apolipoprotein E deposition and astrogliosis are associated with maturation of beta-amyloid plaques in betaAPPswe transgenic mouse: Implications for the pathogenesis of Alzheimer's disease. Brain Res 900:48-56.
60. Theodosis DT, Piet R, Poulain DA, Oliet SH (2004) Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules. Neurochem Int 45:491-501.
61. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Wang X, Zielke HR, Kang J, Nedergaard M (2005) An astrocytic basis of epilepsy. Nat Med 11:973-981.
62. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788-794.
63. Unger JW (1998) Glial reaction in aging and Alzheimer's disease. Microsc Res Tech 43:24-28.
64. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640.
65. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, NedergaardM (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821-827.
66. Weigert C (1895) Beitrage zur kenntnis der normalen menshlichen neuroglia. Frankfurt: Moritz Diesterweg.
67. Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M, Ellisman MH, Pekny M (2006) Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA 103:17513-17518.
68. Willmore LJ, Sypert GW, Munson JB (1978) Recurrent seizures induced by cortical iron injection: a model of posttraumatic epilepsy. Ann Neurol 4:329-336.
69. Willmore LJ, Hiramatsu M, Kochi H, Mori A (1983) Formation of superoxide radicals after FeCl3 injection into rat isocortex. Brain Res 277:393-396.
70. Wuarin JP, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85:1067-1077.
71. Zha XM, Green SH, Dailey ME (2005) Regulation of hippocampal synapse remodeling by epileptiform activity. Mol Cell Neurosci 29:494-506.
72. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, MessingA (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187:36-42.