Glutamatergic and morphological alterations associated with early life seizure-induced preconditioning in young rats

European Journal of Neuroscience

Volumn 32, Issue 11, 2010, Pages 1897-1911

  Saghyan, A ^a   LaTorre, G N ^a   Keesey, R ^b   Sharma, A ^a   Mehta, V ^a   Rudenko, V ^a   Hallas, B H ^a   Rafiuddin, A ^a   Goldstein, B ^a   Friedman, L K ^a,b  

^a NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^b SETON HALL UNIVERSITY   (United States)

Author keywords

Calcium; Development; Hippocampus; NMDA receptor; Resistance; Seizures

Indexed keywords

CALCIUM ION; KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; DENDRITE; DENSITY; DENTATE GYRUS; DEPLETION; DOWN REGULATION; EPILEPSY; GENE EXPRESSION REGULATION; GOLGI STAIN; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MORPHOLOGY; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; SUBICULUM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; CA1 REGION, HIPPOCAMPAL; CALCIUM; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLUTAMIC ACID; KAINIC ACID; NEURONS; PREGNANCY; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; STATUS EPILEPTICUS;

EID: 78649696138     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07464.x     Document Type: Article

References (80)

1. Albala, B.J., Moshe, S.L. & Okada, R. (1984) Kainic acid-induced seizures: a developmental study. Dev. Brain Res., 315, 139-148.
2. André, V., Ferrandon, A., Marescaux, C. & Nehlig, A. (2000) 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, 469-481.
3. Badea, T., Goldberg, J., Mao, B. & Yuste, R. (2001) Calcium imaging of epileptiform events with single-cell resolution. J. Neurobiol., 48, 215-227.
4. Berg, M., Bruhn, T., Frandsen, A., Schousboe, A. & Diemer, N.H. (1995) Kainic acid-induced seizures and brain damage in the rat: role for calcium homeostasis. J. Neurosci. Res., 40, 641-646.
5. Bickler, P.E. & Fahlman, C.S. (2004) Moderate increases in intracellular calcium activate neuroprotective signals in hippocampal neurons. Neuroscience, 127, 673-683.
6. Bo, T., Jiang, Y., Cao, H., Wang, J. & Wu, X. (2004) Long-term effects of seizures in neonatal rats on spatial learning ability and N-methyl-D-aspartate receptor expression in the brain. Brain Res. Dev. Brain Res., 152, 137-142.
7. Boeck, C.R., Ganzella, M., Lottermann, A. & Vendite, D. (2004) NMDA preconditioning protects against seizures and hippocampal neurotoxicity induced by quinolinic acid in mice. Epilepsia, 45, 745-750.
8. Boeck, C.R., Kroth, E.H., Bronzatto, M.J. & Vendite, D. (2005) Adenosine receptors co-operate with NMDA preconditioning to protect cerebellar granule cells against glutamate neurotoxicity. Neuropharmacology, 49, 17-24.
9. Borges, K., Shaw, R. & Dingledine, R. (2007) Gene expression changes after seizure preconditioning in the three major hippocampal cell layers. Neurobiol. Dis., 26, 66-77.
10. Cambonie, G., Hirbec, H., Michaud, M., Kamenka, J.M. & Barbanel, G. (2004) Prenatal infection obliterates glutamate-related protection against free hydroxyl radicals in neonatal rat brain. J. Neurosci. Res., 75, 125-132.
11. Choi, D.W. (1995) Calcium: still center stage in hypoxic-ischemic neuronal death. Trends Neurosci., 18, 58-60.
12. Denk, W., Delaney, K.R., Gelperin, A., Kleinfeld, D., Strowbridge, B.W., Tank, D.W. & Yuste, R. (1994) Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy. J. Neurosci. Methods, 54, 151-162.
13. Dingledine, R., Borges, K., Bowie, D. & Trynelis, S.F. (1999) The glutamate receptor ion channels. Pharmacol. Rev., 74, 723-760.
14. Doriat, J.F., Koziel, V., Humbert, A. & Daval, J. (1999) Repeated seizure-associated long-lasting changes of N-methyl-D-aspartate receptor properties in the developing rat brain. Int. J. Dev. Neurosci., 17, 369-376.
15. +: implications for neurodegeneration. J. Neurochem., 63, 584-591.
16. Fishbein, I. & Segal, M. (2007) Miniature synaptic currents become neurotoxic to chronically silenced neurons. Cereb. Cortex, 17, 1292-1306.
17. Flint, A.C., Maisch, U.S., Weishaupt, J.H., Kriegstein, A.R. & Monyer, H. (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci., 17, 2469-2476.
18. 2+ influx but not Trk activation. J. Neurosci., 15, 643-664.
19. Franklin, J.L. & Johnson, E.M Jr (1992) Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci., 15, 501-508.
20. Franklin, J.L. & Johnson, E.M. Jr (1994) Elevated intracellular calcium blocks programmed neuronal death. Ann. N. Y. Acad. Sci., 747, 195-204.
21. Friedman, L.K. (1998) Selective reduction of GluR2(B) protein in adult hippocampal CA3 neurons following status epilepticus but prior to cell loss. Hippocampus, 8, 511-525.
22. Friedman, L.K. & Segal, M. (2010) Early exposure of cultured hippocampal neurons to excitatory amino acids protects from later excitotoxicity. Int. J. Dev. Neurosci., 28, 195-205.
23. Friedman, L.K., Pellegrini-Giampietro, D.E., Sperber, E.F., Bennett, M.V.L., Moshé, S.L. & Zukin, R.S. (1994) Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study. J. Neurosci., 14, 2697-2707.
24. Friedman, L.K., Sperber, E.F., Moshé, S.L., Bennett, M.V.L. & Zukin, R.S. (1997) Developmental regulation of glutamate and GABAA receptor gene expression in rat hippocampus following kainate-induced status epilepticus. Dev. Neurosci., 19, 529-542.
25. 2+]i surge and neurotoxicity. Int. Neurochem., 43, 179-189.
26. Friedman, L.K., Avallone, J., Magrys, B. & Liu, H. (2007) Age-dependent effects of seizures on AMPA receptors. Dev. Neurosci., 29, 427-437.
27. 2+ accumulations following status epilepticus. Int. J. Dev. Neurosci., 26, 779-790.
28. Gallyas, F., Wolff, J.R., Böttcher, W.H. & Zaborszky, L. (1980) A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol., 55, 299-306.
29. Galvan, C.D., Hrachovy, R.A., Smith, K.L. & Swann, J.W. (2000) Blockade of neuronal activity during hippocampal development produces a chronic focal epilepsy in the rat. J. Neurosci., 20, 2904-2916.
30. González-Burgos, I., López-Vázquez, M.A. & Beas-Zárate, C. (2004) Density, but not shape, of hippocampal dendritic spines varies after a seizure-inducing acute dose of monosodium glutamate in rats. Neurosci. Lett., 363, 22-24.
31. Gonzalez-Zulueta, M., Feldman, A., Klesse, L., Kalb, R., Dillman, J., Parada, L., Dawson, T. & Dawson, V. (2000) Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc. Natl. Acad. Sci. USA, 97, 436-441.
32. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem., 260, 3440-3450.
33. Guthrie, P.B., Segal, M. & Kater, S.B. (1991) Independent regulation of calcium revealed by imaging dendritic spines. Nature, 354, 76-80.
34. Hamon, B. & Heinemann, U. (1988) Developmental changes in neuronal sensitivity to excitatory amino acids in area CA1 of the rat hippocampus. Brain Res., 466, 286-290.
35. Hatazaki, S., Bellver-Estelles, C., Jimenez-Mateos, E.M., Meller, R., Bonner, C., Murphy, N., Matsushima, S., Taki, W., Prehn, J.H.M., Simon, R.P. & Henshall, D.C. (2007) Microarray profile of seizure damage-refractory hippocampal CA3 in a mouse model of epileptic preconditioning. Neuroscience, 150, 467-477.
36. Hayashi, T., Saito, A., Okuno, S., Ferrand-Drake, M. & Chan, P.H. (2003) Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J. Cereb. Blood Flow Metab., 23, 949-961.
37. Hayashi, T., Saito, A., Okuno, S., Ferrand-Drake, M., Dodd, R.L. & Chan, P.H. (2005) Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons. J. Cereb. Blood Flow Metab., 25, 41-53.
38. 2+ from intracellular stores and is prevented by estradiol. Eur. J. Neurosci., 24, 3008-3016.
39. Holmes, G.L. & Thompson, J.L. (1988) Effects of kainic acid on seizure susceptibility in the developing brain. Dev. Brain Res., 39, 51-59.
40. Huntley, G.W., Vickers, J.C. & Morrison, J.H. (1994) Cellular and synaptic localization of NMDA and non-NMDA receptor subunits in neocortex: organizational features related to cortical circuitry, function and disease. Trends Neurosci., 17, 536-543.
41. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem., 268, 2836-2843.
42. Isokawa, M. (1997) Preservation of dendrites with the presence of reorganized mossy fiber collaterals in hippocampal dentate granule cells in patients with temporal lobe epilepsy. Brain Res., 744, 339-343.
43. Isokawa, M. (1998) Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci. Lett., 258, 73-76.
44. Jiang, W., Van Cleemput, J., Sheerin, A.H., Ji, S.P., Zhang, Y., Saucier, D.M., Corcoran, M.E. & Zhang, X. (2005) Involvement of extracellular regulated kinase and p38 kinase in hippocampal seizure tolerance. J. Neurosci. Res., 81, 581-588.
45. Jimenez-Mateos, E.M., Hatazaki, S., Johnson, E.B., Bellver-Estelles, C., Mouri, G., Bonner, C., Prehn, J.H., Meller, R., Simon, R.P. & Henshall, D.C. (2008) Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol. Dis., 32, 442-453.
46. Jones, N.M. & Bergeron, M. (2004) Hypoxia-induced ischemic tolerance in neonatal rat brain involves enhanced ERK1/2 signaling. J. Neurochem., 89, 157-167.
47. Kelly, M.E. & McIntyre, D.C. (1994) Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid induced status epilepticus. Brain Res., 634, 245-256.
48. Khaspekov, L., Shamloo, M., Victorov, I. & Wieloch, T. (1998) Sublethal in vitro glucose-oxygen deprivation protects cultured hippocampal neurons against a subsequent severe insult. Neuroreport, 9, 1273-1276.
49. Kjoller, C. & Diemer, N.H. (2000) GluR2 protein synthesis and metabolism in rat hippocampus following transient and ischemic tolerance induction. Neurochem. Int., 37, 7-15.
50. Kondratyev, A., Sahibzada, N. & Gale, K. (2001) Electroconvulsive shock exposure prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res. Mol. Brain Res., 91, 1-13.
51. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M. & Mishina, M. (1992) Molecular diversity of the NMDA receptor channel. Nature, 358, 36-41.
52. Liu, H., Kaur, J., Dashtipour, K., Kinyamu, R., Ribak, C.E. & Friedman, L.K. (2003) Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticosteroid level. Exp. Neurol., 184, 196-213.
53. Liu, H., Friedman, L.K. & Kaur, J. (2006) Perinatal seizures preferentially protect CA1 neurons from seizure-induced damage in prepubescent rats. Seizure, 15, 1-16.
54. Mancuso, J., Sagyhan, A., La Torre, G.N., Mehta, V.A., Iacobas, D.A., Iacobas, S., Spray, D. & Friedman, L.K. (2009) Mechanisms underlying early-life seizure-induced protection. 2009 Neurosci. Meeting Planner Abstract, 438.5/N1.
55. Marini, A.M. & Paul, S.M. (1993) Induction of a neuroprotective state in cerebellar granule cells following activation of N-methyl-D-aspartate receptors. Ann. NY Acad. Sci., 679, 253-259.
56. Monyer, H., Seeburg, P.H. & Wisden, W. (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron, 6, 799-810.
57. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. & Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 3, 529-540.
58. 2+ mobilization in the CA1 area of hippocampal slices from immature and mature rats during ischemia or glucose deprivation. Brain Res., 769, 158-162.
59. Nilsen, J. & Brinton, R.D. (2003) Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc. Natl. Acad. Sci. USA, 100, 10506-10511.
60. Oray, S., Majewska, A. & Sur, M. (2006) Effects of synaptic activity on dendritic spine motility of developing cortical layer V pyramidal neurons. Cereb. Cortex, 16, 730-741.
61. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, New York.
62. 2+ permeable AMPA receptors in neurological disorders. Trends Neurosci., 20, 464-470.
63. + ATP channel and protein kinase C. Neuroscience, 89, 453-459.
64. Pugliese, A.M., Latini, S., Corradetti, R. & Pedata, F. (2003) Brief, repeated, oxygen-glucose deprivation episodes protect neurotransmission from a longer ischemic episode in the in vitro hippocampus: role of adenosine receptors. Br. J. Pharmacol., 140, 305-314.
65. Van Rensburg, R., Errington, D.R., Ennaceur, A., Lees, G., Obrenovitch, T.P. & Chazot, P.L. (2009) A new model for the study of high-K(+)-induced preconditioning in cultured neurones: role of N-methyl-d-aspartate and alpha7-nicotinic acetylcholine receptors. J. Neurosci. Methods, 177, 311-316.
66. Riva, M.A., Tascedda, F.Molteni, R. & Racagni, G. (1994) Regulation of NMDA receptor subunit mRNA expression in the rat brain during postnatal development. Brain Res. Mol. Brain Res., 25, 209-216.
67. i reveals presence of voltage-gated calcium channels in dendritic spines of cultured hippocampal neurons. J. Neurophysiol., 74, 484-488.
68. Segal, M., Greenberger, V. & Korkotian, E. (2003) Formation of dendritic spines in cultured striatal neurons depends on excitatory afferent activity. Eur. J. Neurosci., 17, 2573-2585.
69. 2+ signaling in rat cortex. Acta Neurobiol. Exp. (Wars), 68, 169-179.
70. Shamloo, M., Rytter, A. & Wieloch, T. (1999) Activation of the extracellular signal-regulated protein kinase cascade in the hippocampal CA1 region in a rat model of global cerebral ischemic preconditioning. Neuroscience, 93, 81-88.
71. Smith, A.J., Stone, T.W. & Smith, R.A. (2008) Preconditioning with NMDA protects against toxicity of 3-nitropropionic acid or glutamate in cultured cerebellar granule neurons. Neurosci. Lett., 440, 294-298.
72. Sperber, E.F., Velísková, J., Germano, I.M., Friedman, L.K. & Moshé, S.L. (1999) Age-dependent vulnerability to seizures. Adv. Neurol., 79, 161-169.
73. Stagliano, N.E., Pérez-Pinzón, M.A., Moskowitz, M.A. & Huang, P.L. (1999) Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J. Cereb. Blood Flow Metab., 19, 757-761.
74. Swann, J.W., Smith, K.L. & Lee, C.L. (2001) Neuronal activity and the establishment of normal and epileptic circuits during brain development. Int. Rev. Neurobiol., 45, 89-118.
75. Tandon, P., Yang, Y., Das, K., Holmes, G.L. & Stafstrom, C.E. (1999) Neuroprotective effects of brain-derived neurotrophic factor in seizures during development. Neuroscience, 91, 293-303.
76. Tauskela, J.S., Brunette, E., Monette, R., Comas, T. & Morley, P. (2003) Preconditioning of cortical neurons by oxygen-glucose deprivation: tolerance induction through abbreviated neurotoxic signaling. Am. J. Physiol., Cell Physiol., 285, C899-C911.
77. Tremblay, E., Roisin, M.P., Represa, A., Charriaut-Marlangue, C. & Ben-Ari, Y. (1988) Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Res., 461, 393-396.
78. Uysal, N., Gonenc, S., Acikgoz, O., Pekçetin, C., Kayatekin, B.M., Sonmez, A. & Semin, I. (2005) Age-dependent effects of maternal deprivation on oxidative stress in infant rat brain. Neurosci. Lett., 384, 98-101.
79. Watanabe, M., Fukaya, M., Sakimura, K. & Manabe, T. (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fiber recipient layer) of mouse hippocampal subfield. Eur. J. Neurosci., 10, 478-487.
80. Yuste, R., Majewska, A., Cash, S.S. & Denk, W. (1999) Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J. Neurosci., 19, 1976-1987.