Hippocampal damage after intra-amygdala kainic acid-induced status epilepticus and seizure preconditioning-mediated neuroprotection in SJL mice

Epilepsy Research

Volumn 88, Issue 2-3, 2010, Pages 151-161

  Tanaka, Katsuhiro ^a,b   Jimenez Mateos, Eva M ^a   Matsushima, Satoshi ^b   Taki, Waro ^b   Henshall, David C ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; C57BL 6; Epilepsy; Hippocampal sclerosis; Kainate; Tolerance

Indexed keywords

KAINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EPILEPTIC STATE; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PHYSICAL TOLERANCE; PRIORITY JOURNAL; SEIZURE; STRAIN DIFFERENCE; SWISS JAMES LAMBERT MOUSE;

AMYGDALA; ANIMALS; CELL DEATH; CYTOPROTECTION; ELECTRODES, IMPLANTED; HIPPOCAMPUS; KAINIC ACID; MICE; MICROINJECTIONS; NEURONS; NEUROPROTECTIVE AGENTS; SCLEROSIS; SEIZURES; STATUS EPILEPTICUS;

EID: 75849128324     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2009.10.012     Document Type: Article

References (56)

1. Andre V., Ferrandon A., Marescaux C., and Nehlig A. The lesional and epileptogenic consequences of lithium-pilocarpine-induced status epilepticus are affected by previous exposure to isolated seizures: effects of amygdala kindling and maximal electroshocks. Neuroscience 99 (2000) 469-481
2. Araki T., Simon R.P., Taki W., Lan J.-Q., and Henshall D.C. Characterization of neuronal death induced by focally evoked limbic seizures in the C57BL/6 mouse. J. Neurosci. Res. 69 (2002) 614-621
3. Barone F.C., White R.F., Spera P.A., Ellison J., Currie R.W., Wang X., and Feuerstein G.Z. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29 (1998) 1937-1950
4. Ben-Ari Y., Tremblay E., and Ottersen O.P. Injections of kainic acid into the amygdaloid complex of the rat: an electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience 5 (1980) 515-528
5. Ben-Ari Y., Tremblay E., Ottersen O.P., and Meldrum B.S. The role of epileptic activity in hippocampal and "remote" cerebral lesions induced by kainic acid. Brain Res. 191 (1980) 79-97
6. Blondeau N., Widmann C., Lazdunski M., and Heurteaux C. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J. Neurosci. 21 (2001) 4668-4677
7. Boeck C.R., Ganzella M., Lottermann A., and Vendite D. NMDA preconditioning protects against seizures and hippocampal neurotoxicity induced by quinolinic acid in mice. Epilepsia 45 (2004) 745-750
8. Borges K., Shaw R., and Dingledine R. Gene expression changes after seizure preconditioning in the three major hippocampal cell layers. Neurobiol. Dis. 26 (2007) 66-77
9. Bronisz A., Sharma S.M., Hu R., Godlewski J., Tzivion G., Mansky K.C., and Ostrowski M.C. Microphthalmia-associated transcription factor interactions with 14-3-3 modulate differentiation of committed myeloid precursors. Mol. Biol. Cell 17 (2006) 3897-3906
10. Cantallops I., and Routtenberg A. Kainic acid induction of mossy fiber sprouting: dependence on mouse strain. Hippocampus 10 (2000) 269-273
11. Curia G., Longo D., Biagini G., Jones R.S., and Avoli M. The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 172 (2008) 143-157
12. Dirnagl U., Simon R.P., and Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26 (2003) 248-254
13. El Bahh B., Auvergne R., Lere C., Brana C., Le Gal La Salle G., and Rougier A. Decreased epileptic susceptibility correlates with neuropeptide Y overexpression in a model of tolerance to excitotoxicity. Brain Res. 894 (2001) 209-217
14. El Bahh B., Lurton D., Sundstrom L.E., and Rougier A. Induction of tolerance and mossy fibre neuropeptide-Y expression in the contralateral hippocampus following a unilateral intrahippocampal kainic acid injection in the rat. Neurosci. Lett. 227 (1997) 135-139
15. Fuller J.L., and Collins R.L. Mice unilaterally sensitized for audiogenic seizures. Science 162 (1968) 1295
16. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 7 (2006) 437-448
17. Golden G.T., Ferraro T.N., Smith G.G., Snyder R.L., Jones N.L., and Berrettini W.H. Acute cocaine-induced seizures: differential sensitivity of six inbred mouse strains. Neuropsychopharmacology 24 (2001) 291-299
18. Hatazaki S., Bellver-Estelles C., Jimenez-Mateos E.M., Meller R., Bonner C., Murphy N., Matsushima S., Taki W., Prehn J.H., Simon R.P., and Henshall D.C. Microarray profile of seizure damage-refractory hippocampal CA3 in a mouse model of epileptic preconditioning. Neuroscience 150 (2007) 467-477
19. Jimenez-Mateos E.M., Hatazaki S., Johnson M.B., Bellver-Estelles C., Mouri G., Bonner C., Prehn J.H., Meller R., Simon R.P., and Henshall D.C. Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol. Dis. 32 (2008) 442-453
20. Kasugai M., Akaike K., Imamura S., Matsukubo H., Tojo H., Nakamura M., Tanaka S., and Sano A. Differences in two mice strains on kainic acid-induced amygdalar seizures. Biochem. Biophys. Res. Commun. 357 (2007) 1078-1083
21. Kelly M.E., and McIntyre D.C. Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Res. 634 (1994) 245-256
22. Kienzler F., Jedlicka P., Vuksic M., Deller T., and Schwarzacher S.W. Excitotoxic hippocampal neuron loss following sustained electrical stimulation of the perforant pathway in the mouse. Brain Res. 1085 (2006) 195-198
23. Kienzler F., Norwood B.A., and Sloviter R.S. Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J. Comp. Neurol. 515 (2009) 181-196
24. Kirino T. Ischemic tolerance. J. Cereb. Blood Flow Metab. 22 (2002) 1283-1296
25. Kondratyev A., Sahibzada N., and Gale K. Electroconvulsive shock exposure prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res. Mol. Brain Res. 91 (2001) 1-13
26. Lere C., El Bahh B., Le Gal La Salle G., and Rougier A. A model of 'epileptic tolerance' for investigating neuroprotection, epileptic susceptibility and gene expression-related plastic changes. Brain Res. Brain Res. Protoc. 9 (2002) 49-56
27. Lorenzana A., Chancer Z., and Schauwecker P.E. A quantitative trait locus on chromosome 18 is a critical determinant of excitotoxic cell death susceptibility. Eur. J. Neurosci. 25 (2007) 1998-2008
28. Mathern G.W., Babb T.L., and Armstrong D.L. Hippocampal sclerosis. In: Engel J.J., and Pedley T.A. (Eds). Epilepsy: A Comprehensive Textbook (1997), Lippincott-Raven Publishers, Philadelphia 133-155
29. McIntyre D. The kindling phenomenon. In: Pitkanen A., Schwartzkroin P.A., and Moshe S.L. (Eds). Models of Seizures and Epilepsy (2006), Elsevier, San Diego 351-363
30. McLin J.P., and Steward O. Comparison of seizure phenotype and neurodegeneration induced by systemic kainic acid in inbred, outbred, and hybrid mouse strains. Eur. J. Neurosci. 24 (2006) 2191-2202
31. Meller R., Cameron J.A., Torrey D.J., Clayton C.E., Ordonez A.N., Henshall D.C., Minami M., Schindler C.K., Saugstad J.A., and Simon R.P. Rapid degradation of Bim by the ubiquitin-proteasome pathway mediates short-term ischemic tolerance in cultured neurons. J. Biol. Chem. 281 (2006) 7429-7436
32. Meller R., Thompson S.J., Lusardi T.A., Ordonez A.N., Ashley M.D., Jessick V., Wang W., Torrey D.J., Henshall D.C., Gafken P.R., Saugstad J.A., Xiong Z.G., and Simon R.P. Ubiquitin proteasome-mediated synaptic reorganization: a novel mechanism underlying rapid ischemic tolerance. J. Neurosci. 28 (2008) 50-59
33. Mouri G., Jimenez-Mateos E., Engel T., Dunleavy M., Hatazaki S., Paucard A., Matsushima S., Taki W., and Henshall D.C. Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res. 1213 (2008) 140-151
34. Muller C.J., Groticke I., Hoffmann K., Schughart K., and Loscher W. Differences in sensitivity to the convulsant pilocarpine in substrains and sublines of C57BL/6 mice. Genes Brain Behav. 8 (2009) 481-492
35. Murphy N., Bonner H.P., Ward M.W., Murphy B.M., Prehn J.H., and Henshall D.C. Depletion of 14-3-3 zeta elicits endoplasmic reticulum stress and cell death, and increases vulnerability to kainate-induced injury in mouse hippocampal cultures. J. Neurochem. 106 (2008) 978-988
36. Najm I.M., Hadam J., Ckakraverty D., Mikuni N., Penrod C., Sopa C., Markarian G., Luders H.O., Babb T., and Baudry M. A short episode of seizure activity protects from status epilepticus-induced neuronal damage in rat brain. Brain Res. 810 (1998) 72-75
37. Namgung U., Valcourt E., and Routtenberg A. Long-term potentiation in vivo in the intact mouse hippocampus. Brain Res. 689 (1995) 85-92
38. Ogita K., Okuda H., Yamamoto Y., Nishiyama N., and Yoneda Y. In vivo neuroprotective role of NMDA receptors against kainate-induced excitotoxicity in murine hippocampal pyramidal neurons. J. Neurochem. 85 (2003) 1336-1346
39. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates. second ed. (2001), Elsevier, San Diego, CA
40. Perez-Pinzon M.A., and Born J.G. Rapid preconditioning neuroprotection following anoxia in hippocampal slices: role of the K+ ATP channel and protein kinase C. Neuroscience 89 (1999) 453-459
41. Pitkanen A., Pikkarainen M., Nurminen N., and Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat: a review. Ann. N.Y. Acad. Sci. 911 (2000) 369-391
42. Pitkanen A., Savander V., and LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci. 20 (1997) 517-523
43. Pitkanen A., Tuunanen J., Kalviainen R., Partanen K., and Salmenpera T. Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res. 32 (1998) 233-253
44. Sasahira M., Lowry T., Simon R.P., and Greenberg D.A. Epileptic tolerance: prior seizures protect against seizure-induced neuronal injury. Neurosci. Lett. 185 (1995) 95-98
45. Schauwecker P.E. Complications associated with genetic background effects in models of experimental epilepsy. Prog. Brain Res. 135 (2002) 139-148
46. Schauwecker P.E. Modulation of cell death by mouse genotype: differential vulnerability to excitatory amino acid-induced lesions. Exp. Neurol. 178 (2002) 219-235
47. Schauwecker P.E. Differences in ionotropic glutamate receptor subunit expression are not responsible for strain-dependent susceptibility to excitotoxin-induced injury. Brain Res. Mol. Brain Res. 112 (2003) 70-81
48. Schauwecker P.E., and Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4103-4108
49. Schauwecker P.E., Williams R.W., and Santos J.B. Genetic control of sensitivity to hippocampal cell death induced by kainic acid: a quantitative trait loci analysis. J. Comp. Neurol. 477 (2004) 96-107
50. Shinoda S., Araki T., Lan J.Q., Schindler C.K., Simon R.P., Taki W., and Henshall D.C. Development of a model of seizure-induced hippocampal injury with features of programmed cell death in the BALB/c mouse. J. Neurosci. Res. 76 (2004) 121-128
51. Sloviter R.S. Hippocampal epileptogenesis in animal models of mesial temporal lobe epilepsy with hippocampal sclerosis: the importance of the "latent period" and other concepts. Epilepsia 49 Suppl. 9 (2008) 85-92
52. Stenzel-Poore M.P., Stevens S.L., King J.S., and Simon R.P. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38 (2007) 680-685
53. Stenzel-Poore M.P., Stevens S.L., Xiong Z., Lessov N.S., Harrington C.A., Mori M., Meller R., Rosenzweig H.L., Tobar E., Shaw T.E., Chu X., and Simon R.P. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362 (2003) 1028-1037
54. van Groen T., Miettinen P., and Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13 (2003) 133-149
55. Wahlsten D., Metten P., and Crabbe J.C. Survey of 21 inbred mouse strains in two laboratories reveals that BTBR T/+ tf/tf has severely reduced hippocampal commissure and absent corpus callosum. Brain Res. 971 (2003) 47-54
56. Wieser H.G. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45 (2004) 695-714