Epilepsy Research
Volume 88, Issue 2 , Pages 151-161 , February 2010

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

  • Katsuhiro Tanaka

      Affiliations

    • Department of Physiology & Medical Physics, Royal College of Surgeons in Ireland, 123 St. Stephen's Green, Dublin 2, Ireland
    • Department of Neurosurgery, Mie University School of Medicine, Tsu, Mie, Japan
  • ,
  • Eva M. Jimenez-Mateos

      Affiliations

    • Department of Physiology & Medical Physics, Royal College of Surgeons in Ireland, 123 St. Stephen's Green, Dublin 2, Ireland
  • ,
  • Satoshi Matsushima

      Affiliations

    • Department of Neurosurgery, Mie University School of Medicine, Tsu, Mie, Japan
  • ,
  • Waro Taki

      Affiliations

    • Department of Neurosurgery, Mie University School of Medicine, Tsu, Mie, Japan
  • ,
  • David C. Henshall

      Affiliations

    • Department of Physiology & Medical Physics, Royal College of Surgeons in Ireland, 123 St. Stephen's Green, Dublin 2, Ireland
    • Corresponding Author InformationCorresponding author. Tel.: +353 14028629; fax: +353 14022447.

Received 30 September 2009 ,Revised 20 October 2009 ,Accepted 21 October 2009.

References 

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

PII: S0920-1211(09)00317-9

doi: 10.1016/j.eplepsyres.2009.10.012

Epilepsy Research
Volume 88, Issue 2 , Pages 151-161 , February 2010