CNTF-mediated preactivation of astrocytes attenuates neuronal damage and epileptiform activity in experimental epilepsy

Experimental Neurology

Volumn 236, Issue 1, 2012, Pages 141-150

  Bechstein, Matthias ^a   Häussler, Ute ^a   Neef, Matthias ^a   Hofmann, Hans Dieter ^a   Kirsch, Matthias ^a   Haas, Carola A ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cell death; Ciliary neurotrophic factor; EEG; Fast ripples; Granule cell dispersion; Hippocampus; Kainate; Temporal lobe epilepsy

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DAMAGE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE SEVERITY; EPILEPTIC DISCHARGE; EPILEPTIC STATE; EPILEPTOGENESIS; EXCITOTOXICITY; IMMUNOREACTIVITY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL LESION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA SYNTHESIS;

ANIMALS; ASTROCYTES; CILIARY NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPROTECTIVE AGENTS;

EID: 84861665759     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.04.009     Document Type: Article

References (56)

1. Beurrier C., Faideau M., Bennouar K.E., Escartin C., Kerkerian-Le Goff L., Bonvento G., Gubellini P. Ciliary neurotrophic factor protects striatal neurons against excitotoxicity by enhancing glial glutamate uptake. PLoS One 2010, 5:e8550.
2. Binder D.K., Steinhäuser C. Functional changes in astroglial cells in epilepsy. Glia 2006, 54:358-368.
3. Blümcke I., Thom M., Wiestler O.D. Ammon's horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathol. 2002, 12:199-211.
4. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 1999, 89:717-729.
5. Bragin A., Engel J., Staba R.J. High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 2010, 23:151-156.
6. Chang B.S., Lowenstein D.H. Epilepsy. N. Engl. J. Med. 2003, 349:1257-1266.
7. Darnell J.E., Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994, 264:1415-1421.
8. Dirnagl U., Simon R.P., Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 2003, 26:248-254.
9. Dittrich F., Thoenen H., Sendtner M. Ciliary neurotrophic factor: pharmacokinetics and acute-phase response in rat. Ann. Neurol. 1994, 35:151-163.
10. Duveau V., Madhusudan A., Caleo M., Knüsel I., Fritschy J.M. Impaired reelin processing and secretion by Cajal-Retzius cells contributes to granule cell dispersion in a mouse model of temporal lobe epilepsy. Hippocampus 2011, 21:935-944.
11. Emerich D.F., Thanos C.G. Intracompartmental delivery of CNTF as therapy for Huntington's disease and retinitis pigmentosa. Curr. Gene Ther. 2006, 6:147-159.
12. Escartin C., Brouillet E., Gubellini P., Trioulier Y., Jacquard C., Smadja C., Knott G.W., Kerkerian-Le Goff L., Deglon N., Hantraye P., Bonvento G. Ciliary neurotrophic factor activates astrocytes, redistributes their glutamate transporters GLAST and GLT-1 to raft microdomains, and improves glutamate handling in vivo. J. Neurosci. 2006, 26:5978-5989.
13. Escartin C., Pierre K., Colin A., Brouillet E., Delzescaux T., Guillermier M., Dhenain M., Deglon N., Hantraye P., Pellerin L., Bonvento G. Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J. Neurosci. 2007, 27:7094-7104.
14. Foffani G., Uzcategui Y.G., Gal B., Menendez de la Prida L. Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 2007, 55:930-941.
15. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 2006, 7:437-448.
16. Haas C.A., Frotscher M. Reelin deficiency causes granule cell dispersion in epilepsy. Exp. Brain Res. 2010, 200:141-149.
17. Haas C.A., Dudeck O., Kirsch M., Huszka C., Kann G., Pollak S., Zentner J., Frotscher M. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 2002, 22:5797-5802.
18. Häussler U., Bielefeld L., Froriep U.P., Wolfart J., Haas C.A. Septotemporal position in the hippocampal formation determines epileptic and neurogenic activity in temporal lobe epilepsy. Cereb. Cortex 2012, 22:26-36.
19. Heinrich C., Nitta N., Flubacher A., Müller M., Fahrner A., Kirsch M., Freiman T., Suzuki F., Depaulis A., Frotscher M., Haas C.A. Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 2006, 26:4701-4713.
20. Herrmann J.E., Imura T., Song B., Qi J., Ao Y., Nguyen T.K., Korsak R.A., Takeda K., Akira S., Sofroniew M.V. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J. Neurosci. 2008, 28:7231-7243.
21. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990, 535:195-204.
22. Jacobs J., Levan P., Chatillon C.E., Olivier A., Dubeau F., Gotman J. High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. Brain 2009, 132:1022-1037.
23. Jiruska P., Finnerty G.T., Powell A.D., Lofti N., Cmejla R., Jefferys J.G. Epileptic high-frequency network activity in a model of non-lesional temporal lobe epilepsy. Brain 2010, 133:1380-1390.
24. Kahn M.A., Ellison J.A., Speight G.J., de Vellis J. CNTF regulation of astrogliosis and the activation of microglia in the developing rat central nervous system. Brain Res. 1995, 685:55-67.
25. Le Van Quyen M., Bragin A. Analysis of dynamic brain oscillations: methodological advances. Trends Neurosci. 2007, 30:365-373.
26. Lere C., El Bahh B., Le Gal La Salle G., Rougier A. A model of 'epileptic tolerance' for investigating neuroprotection, epileptic susceptibility and gene expression-related plastic changes. Brain Res. Brain Res. Protoc. 2002, 9:49-56.
27. Levison S.W., Ducceschi M.H., Young G.M., Wood T.L. Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp. Neurol. 1996, 141:256-268.
28. Marin-Teva J.L., Cuadros M.A., Martin-Oliva D., Navascues J. Microglia and neuronal cell death. Neuron Glia Biol. 2012, 1-16.
29. Mattson M.P., Rychlik B. Glia protect hippocampal neurons against excitatory amino acid-induced degeneration: involvement of fibroblast growth factor. Int. J. Dev. Neurosci. 1990, 8:399-415.
30. Morrison R.S., Wenzel H.J., Kinoshita Y., Robbins C.A., Donehower L.A., Schwartzkroin P.A. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J. Neurosci. 1996, 16:1337-1345.
31. Müller M.C., Osswald M., Tinnes S., Haeussler U., Jacobi A., Förster E., Frotscher M., Haas C.A. Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp. Neurol. 2009, 216:390-397.
32. Okada S., Nakamura M., Katoh H., Miyao T., Shimazaki T., Ishii K., Yamane J., Yoshimura A., Iwamoto Y., Toyama Y., Okano H. Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med. 2006, 12:829-834.
33. Pallud J., Häussler U., Langlois M., Hamelin S., Devaux B., Deransart C., Depaulis A. Dentate gyrus and hilus transection blocks seizure propagation and granule cell dispersion in a mouse model for mesial temporal lobe epilepsy. Hippocampus 2011, 21:334-343.
34. Plamondon H., Blondeau N., Heurteaux C., Lazdunski M. Mutually protective actions of kainic acid epileptic preconditioning and sublethal global ischemia on hippocampal neuronal death: involvement of adenosine A1 receptors and K(ATP) channels. J. Cereb. Blood Flow Metab. 1999, 19:1296-1308.
35. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends Neurosci. 2007, 30:527-535.
36. Riban V., Bouilleret V., Pham-Le B.T., Fritschy J.M., Marescaux C., Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 2002, 112:101-111.
37. Rudge J.S., Li Y., Pasnikowski E.M., Mattsson K., Pan L., Yancopoulos G.D., Wiegand S.J., Lindsay R.M., Ip N.Y. Neurotrophic factor receptors and their signal transduction capabilities in rat astrocytes. Eur. J. Neurosci. 1994, 6:693-705.
38. Sarafian T.A., Montes C., Imura T., Qi J., Coppola G., Geschwind D.H., Sofroniew M.V. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 2010, 5:e9532.
39. Seifert G., Schilling K., Steinhaeuser C. Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat. Rev. Neurosci. 2006, 7:194-206.
40. Seifert G., Carmignoto G., Steinhaeuser C. Astrocyte dysfunction in epilepsy. Brain Res. Rev. 2010, 63:212-221.
41. Shapiro L.A., Perez Z.D., Foresti M.L., Arisi G.M., Ribak C.E. Morphological and ultrastructural features of Iba1-immunolabeled microglial cells in the hippocampal dentate gyrus. Brain Res. 2009, 1266:29-36.
42. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009, 32:638-647.
43. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
44. Stahl N., Yancopoulos G.D. The tripartite CNTF receptor complex: activation and signaling involves components shared with other cytokines. J. Neurobiol. 1994, 25:1454-1466.
45. Suzuki F., Junier M.P., Guilhem D., Sorensen J.C., Onteniente B. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience 1995, 64:665-674.
46. Suzuki F., Heinrich C., Boehrer A., Mitsuya K., Kurokawa K., Matsuda M., Depaulis A. Glutamate receptor antagonists and benzodiazepine inhibit the progression of granule cell dispersion in a mouse model of mesial temporal lobe epilepsy. Epilepsia 2005, 46:193-202.
47. Takahashi D.K., Vargas J.R., Wilcox K.S. Increased coupling altered glutamate transport currents in astrocytes following kainic-acid-induced status epilepticus. Neurobiol. Dis. 2010, 40:573-585.
48. Tinnes S., Schäfer M.K., Flubacher A., Münzner G., Frotscher M., Haas C.A. Epileptiform activity interferes with proteolytic processing of Reelin required for dentate granule cell positioning. FASEB J. 2011, 25:1002-1013.
49. Trendelenburg G., Dirnagl U. Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 2005, 50:307-320.
50. Turnley A.M., Bartlett P.F. Cytokines that signal through the leukemia inhibitory factor receptor-beta complex in the nervous system. J. Neurochem. 2000, 74:889-899.
51. van 't Klooster M.A., Zijlmans M., Leijten F.S., Ferrier C.H., van Putten M.J., Huiskamp G.J. Time-frequency analysis of single pulse electrical stimulation to assist delineation of epileptogenic cortex. Brain 2011, 134:2855-2866.
52. Vincent P., Mulle C. Kainate receptors in epilepsy and excitotoxicity. Neuroscience 2009, 158:309-323.
53. Wallraff A., Koehling R., Heinemann U., Theis M., Willecke K., Steinhaeuser C. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 2006, 26:5438-5447.
54. Wetherington J., Serrano G., Dingledine R. Astrocytes in the epileptic brain. Neuron 2008, 58:168-178.
55. Wilde G.J., Pringle A.K., Wright P., Iannotti F. Differential vulnerability of the CA1 and CA3 subfields of the hippocampus to superoxide and hydroxyl radicals in vitro. J. Neurochem. 1997, 69:883-886.
56. Xia X.G., Hofmann H.D., Deller T., Kirsch M. Induction of STAT3 signaling in activated astrocytes and sprouting septal neurons following entorhinal cortex lesion in adult rats. Mol. Cell. Neurosci. 2002, 21:379-392.