Skip to main content
Log in

Gene Expression Profiling of Seizure Disorders

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Seizure disorders affect a significant percentage of the population, and researchers worldwide continue to work toward a better understanding of what initiates, propagates, and results from aberrant and excessive neuronal excitation. During the past two decades, one aspect of this research effort has been to describe the effects of seizure activity upon neuronal gene expression, with hopes of identifying the molecular mechanisms that underlie subsequent changes in cell function and survival. Here we review this body of work from the perspective of how these gene profiling efforts have evolved, starting with one-by-one analyses of specific gene targets to the more recent use of DNA microarrays to survey literally thousands of genes simultaneously. With regard to the latter, we present some of our own work that suggests that molecular mechanisms contributing to normal brain development are reiterated during seizure-induced network reorganization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Coulter, D. A., McIntyre, D. C., and Loscher, W. 2002. Animal models of limbic epilepsies: what can they tell us? Brain Pathol. 12(2):240–256.

    PubMed  Google Scholar 

  2. White, H. S. 2002. Animal models of epileptogenesis. Neurology. 59 (9 Suppl 5):S7–S14.

    Google Scholar 

  3. Goddard, G. V., McIntyre, D. C., and Leech, C. K. 1969. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 25(3):295–330.

    PubMed  Google Scholar 

  4. Racine, R. J. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32(3):281–294.

    PubMed  Google Scholar 

  5. Racine, R. 1978. Kindling: the first decade. Neurosurgery. 3(2):234–252.

    PubMed  Google Scholar 

  6. Wasterlain, C. G., Morin, A. M., and Jonec, V. 1982. Kindling: a pharmacological approach. Electroencephalogr. Clin. Neurophysiol. Suppl. 36:264–273.

    PubMed  Google Scholar 

  7. Sloviter, R. S. and Damiano, B. P. 1981. Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci. Lett. 24(3):279–284.

    PubMed  Google Scholar 

  8. Sloviter, R. S. 1983. “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res. Bull. 10(5):675–697.

    PubMed  Google Scholar 

  9. Swinyard, E. A. 1969. Laboratory evaluation of antiepileptic drugs. Review of laboratory methods. Epilepsia 10(2):107–119.

    PubMed  Google Scholar 

  10. Squires, R. F., Saederup, E., Crawley, J. N., Skolnick, P., and Paul, S. M. 1984. Convulsant potencies of tetrazoles are highly correlated with actions on GABA/benzodiazepine/picrotoxin receptor complexes in brain. Life Sci. 35(14):1439–1444.

    PubMed  Google Scholar 

  11. Campbell, K. A., Bank, B., and Milgram, N. W. 1984. Epileptogenic effects of electrolytic lesions in the hippocampus: role of iron deposition. Exp. Neurol. 86(3):506–514.

    PubMed  Google Scholar 

  12. Pico, R. M. and Gall, C. M. 1994. Hippocampal epileptogenesis produced by electrolytic iron deposition in the rat dentate gyrus. Epilepsy Res. 19:27–36.

    PubMed  Google Scholar 

  13. Nadler, J. V. 1981. Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 29(20):2031–2042.

    PubMed  Google Scholar 

  14. Cavalheiro, E. A. 1995. The pilocarpine model of epilepsy. Ital. J. Neurol. Sci. 16:33–37.

    Google Scholar 

  15. Ben-Ari, Y. and Cossart, R. 2000. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23(11):580–587.

    PubMed  Google Scholar 

  16. Margerison, J. H. and Corsellis, J. A. 1966. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89(3):499–530.

    PubMed  Google Scholar 

  17. Lowenstein, D. H. 2001. Structural reorganization of hippocampal networks caused by seizure activity. Int. Rev. Neurobiol. 45:209–236.

    PubMed  Google Scholar 

  18. Sutula, T., Cascino, G., Cavazos, J., Parada, I., and Ramirez, L. 1989. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26(3):321–330.

    PubMed  Google Scholar 

  19. Houser, C. R., Miyashiro, J. E., Swartz, B. E., Walsh, G. O., Rich, J. R., and Delgado-Escueta, A. V. 1990. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10(1):267–282.

    PubMed  Google Scholar 

  20. Isokawa, M., Levesque, M. F., Babb, T. L., and Engel, J., Jr. 1993. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J. Neurosci. 13(4):1511–1522.

    PubMed  Google Scholar 

  21. Franck, J., Pokorny, J., Kunkel, D. D., and Schwartzkroin, P. A. 1995. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia. 36:543–558.

    PubMed  Google Scholar 

  22. Tauck, D. and Nadler, J. 1985. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J.Neurosci. 5(4):1016–1022.

    PubMed  Google Scholar 

  23. Sloviter, R. S. 1992. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 137:91–96.

    PubMed  Google Scholar 

  24. Wuarin, J. and Dudek, F. 1996. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J. Neurosci. 16:4438–4448.

    PubMed  Google Scholar 

  25. Ben-Ari, Y. 1985. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14(2):375–403.

    PubMed  Google Scholar 

  26. Cronin, J. and Dudek, F. E. 1988. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474(1):181–184.

    PubMed  Google Scholar 

  27. Mello, L. E., Cavalheiro, E. A., Tan, A. M., Kupfer, W. R., Pretorius, J. K., Babb, T. L., and Finch, D. M. 1993. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34(6):985–995.

    PubMed  Google Scholar 

  28. Sonnenberg, J. L., Mitchelmore, C., Macgregor-Leon, P. F., Hempstead, J., Morgan, J. I., and Curran, T. 1989. Glutamate receptor agonists increase the expression of Fos, Fra, and AP-1 DNA binding activity in the mammalian brain. J. Neurosci. Res. 24(1):72–80.

    PubMed  Google Scholar 

  29. Kaminska, B., Filipkowski, R. K., Zurkowska, G., Lason, W., Przewlocki, R., and Kaczmarek, L. 1994. Dynamic changes in the composition of the AP-1 transcription factor DNA-binding activity in rat brain following kainate-induced seizures and cell death. Eur. J. Neurosci. 6:1558–1566.

    PubMed  Google Scholar 

  30. Hope, B. T., Kelz, M. B., Duman, R. S., and Nestler, E. J. 1994. Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics. J. Neurosci. 14(7):4318–4328.

    PubMed  Google Scholar 

  31. Pennypacker, K. P., Thai, L., Hong, J-S., and McMillian, M. K. 1994. Prolonged expression of AP-1 transcription factors in the rat hippocampus after systemic kainate treatment. J. Neurosci. 14(7):3998–4006.

    PubMed  Google Scholar 

  32. McNamara, J. O., Peper, A. M., and Patrone, V. 1980. Repeated seizures induce long-term increase in hippocampal benzodiazepine receptors. Proc. Natl. Acad. Sci. USA 77(5):3029–3032.

    PubMed  Google Scholar 

  33. Valdes, F., Dasheiff, R. M., Birmingham, F., Crutcher, K. A., and McNamara, J. O. 1982. Benzodiazepine receptor increases after repeated seizures: evidence for localization to dentate granule cells. Proc. Natl. Acad. Sci. USA 79(1):193–197.

    PubMed  Google Scholar 

  34. Shin, C., Pedersen, H. B., and McNamara, J. O. 1985. Gamma-aminobutyric acid and benzodiazepine receptors in the kindling model of epilepsy: a quantitative radiohistochemical study. J.Neurosci. 5(10):2696–2701.

    PubMed  Google Scholar 

  35. Hong, J. S., Wood, P. L., Gillin, J. C., Yang, H. Y., and Costa, E. 1980. Changes of hippocampal metenkephalin content after recurrent motor seizures. Nature 285(5762):231–232.

    PubMed  Google Scholar 

  36. Lason, W., Przewlocka, B., Stala, L., and Przewlocki, R. 1983. Changes in hippocampal immunoreactive dynorphin and neoendorphin content following intra-amygdalar kainic acid-induced seizures. Neuropeptides 3(5):399–404.

    PubMed  Google Scholar 

  37. White, J. D. and Gall, C. M. 1986. Increased enkephalin gene expression in the hippocampus following seizures. NIDA Res. Monogr. 75:393–396.

    PubMed  Google Scholar 

  38. Pitkanen, A., Beal, M. F., Sirvio, J., Swartz, K. J., Mannisto, P.T., and Riekkinen, P. J. 1989. Somatostatin, neuropeptide Y, GABA and cholinergic enzymes in brain of pentylenetetrazol-kindled rats. Neuropeptides 14(3):197–207.

    PubMed  Google Scholar 

  39. Gall, C., Lauterborn, J., Isackson, P., and White, J. 1990. Seizures, neuropeptide regulation, and mRNA expression in the hippocampus. Prog. Brain Res. 83:371–390.

    PubMed  Google Scholar 

  40. McGinty, J. F., Kanamatsu, T., Obie, J., and Hong, J. S. 1986. Modulation of opioid peptide metabolism by seizures: differentiation of opioid subclasses. NIDA Res. Monogr. 71:89–101.

    PubMed  Google Scholar 

  41. Morgan, J. I., Cohen, D. R., Hempstead, J. L., and Curran, T. 1987. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237(4811):192–197.

    PubMed  Google Scholar 

  42. Sonnenberg, J. L., Macgregor-Leon, P. F., Curran, T., and Morgan, J. I. 1989. Dynamic alterations occur in the levels and composition of transcription factor AP-1 complexes after seizure. Neuron 3:359–365.

    PubMed  Google Scholar 

  43. Dragunow, M., Yamada, N., Bilkey, D. K., and Lawlor, P. 1992. Induction of immediate-early gene proteins in dentate granule cells and somatostatin interneurons after hippocampal seizures. Mol. Brain Res. 13(1-;2):119–126.

    PubMed  Google Scholar 

  44. Gass, P., Herdegen, T., Bravo, R., and Kiessling, M. 1992. Induction of immediate early gene encoded proteins in the rat hippocampus after bicuculline-induced seizures: differential expression of KROX-24, Fos and Jun proteins. Neuroscience 48(2):315–324.

    PubMed  Google Scholar 

  45. Elliott, R. C. and Gall, C. M. 2000. Changes in activating protein 1 (AP-1) composition correspond with the biphasic profile of nerve growth factor mRNA expression in rat hippocampus after hilus lesion-induced seizures. J. Neurosci. 20(6):2142–2149.

    PubMed  Google Scholar 

  46. Sonnenberg, J. L., Rauscher III, F. J., Morgan, J. I., and Curran, T. 1989. Regulation of proenkephalin by Fos and Jun. Science. 246:1622–1625.

    PubMed  Google Scholar 

  47. Gonzalez-Martin, C., de Diego, I., Crespo, D., and Fairen, A. 1992. Transient c-fos expression accompanies naturally occurring cell death in the developing interhemispheric cortex of the rat. Brain Res. Dev. Brain Res. 68(1):83–95.

    PubMed  Google Scholar 

  48. Smeyne, R. J., Vendrell, M., Hayward, M., Baker, S. J., Miao, G. G., Schilling, K., Robertson, L. M., Curran, T., and Morgan, J. I. 1993. Continuous c-fos expression precedes programmed cell death in vivo. Nature 363(6425):166–169.

    PubMed  Google Scholar 

  49. Kasof, G. M., Mandelzys, A., Maika, S. D., Hammer, R. E., Curran, T., and Morgan, J. I. 1995. Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats. J. Neurosci. 15(6):4238–4249.

    PubMed  Google Scholar 

  50. Kaczmarek, L. 1992. Expression of c-fos and other genes encoding transcription factors in long-term potentiation. Behav. Neural Biol. 57(3):263–266.

    PubMed  Google Scholar 

  51. Nikolaev, E., Kaminska, B., Tischmeyer, W., Matthies, H., and Kaczmarek, L. 1992. Induction of expression of genes encoding transcription factors in the rat brain elicited by behavioral training. Brain Res. Bull. 28:479–484.

    PubMed  Google Scholar 

  52. Abraham, W. C., Mason, S. E., Demmer, J., Williams, J. M., Richardson, C. L., Tate, W. P., Lawlor, P. A., and Dragunow, M. 1993. Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 56(3):717–727.

    PubMed  Google Scholar 

  53. Dragunow, M. 1996. A role for immediate-early transcription factors in learning and memory. Behav. Genet. 26(3):293–299.

    PubMed  Google Scholar 

  54. Gall, C. M. and Isackson, P. J. 1989. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245:758–761.

    PubMed  Google Scholar 

  55. Lauterborn, J. C., Isackson, P. J., and Gall, C. M. 1994. Seizure-induced increases in NGF mRNA exhibit different time courses across forebrain regions and are biphasic in hippocampus. Exp. Neurol. 125:22–40.

    PubMed  Google Scholar 

  56. Isackson, P. J., Huntsman, M. M., Murray, K. D., and Gall, C. M. 1991. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction different from NGF. Neuron 6:937–948.

    PubMed  Google Scholar 

  57. Dugich-Djordjevic, M. M., Tocco, G., Lapchak, P. A., Pasinetti, G. M., Najm, I., Baudry, M., and Hefti, F. 1992. Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid. Neuroscience 47(2):303–315.

    PubMed  Google Scholar 

  58. Humpel, C., Wetmore, C., and Olson, L. 1993. Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience 53(4):909–918.

    PubMed  Google Scholar 

  59. Gall, C., Lauterborn, J., Bundman, M., Murray, K., and Isackson, P. 1991. Seizures and the regulation of neurotrophic factor and neuropeptide gene expression in brain. Epilepsy Res. Suppl. 4:225–245.

    PubMed  Google Scholar 

  60. Rocamora, N., Palacios, J. M., and Mengod, G. 1992. Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in the rat hippocampus. Brain Res. Mol. Brain Res. 13(1-;2):27–33.

    PubMed  Google Scholar 

  61. Merlio, J., Ernfors, P., Kokaia, Z., Middlemas, D., Bengzon, J., Kokaia, M., Smith, M., Siesjo, B., Hunter, T., Lindvall, O., and Persson, H. 1993. Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron 10(2):151–164.

    PubMed  Google Scholar 

  62. Binder, D. K., Routbort, M. J., and McNamara, J. O. 1999. Immunohistochemical evidence of seizure-induced activation of trk receptors in the mossy fiber pathway of adult rat hippocampus. J. Neurosci. 19(11):4616–4626.

    PubMed  Google Scholar 

  63. Roux, P. P., Colicos, M. A., Barker, P. A., and Kennedy, T. E. 1999. p75 neurotrophin receptor expression is induced in apoptotic neurons after seizure. J. Neurosci. 19(16):6887–6896.

    PubMed  Google Scholar 

  64. Kokaia, Z., Bengzon, J., Metsis, M., Kokaia, M., Persson, H., and Lindvall, O. 1993. Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc. Natl. Acad. Sci. USA 90(14):6711–6715.

    PubMed  Google Scholar 

  65. Kokaia, M., Ernfors, P., Kokaia, Z., Elmer, E., Jaenisch, R., and Lindvall, O. 1995. Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol. 133(2):215–224.

    PubMed  Google Scholar 

  66. Larmet, Y., Reibel, S., Carnahan, J., Nawa, H., Marescaux, C., and Depaulis, A. 1995. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport 6(14):1937–1941.

    PubMed  Google Scholar 

  67. Croll, S. D., Suri, C., Compton, D. L., Simmons, M. V., Yancopoulos, G. D., Lindsay, R. M., Wiegand, S. J., Rudge, J. S., and Scharfman, H. E. 1999. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93(4):1491–1506.

    PubMed  Google Scholar 

  68. Kang, H. and Schuman, E. 1995. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267(5204):1658–1662.

    PubMed  Google Scholar 

  69. Levine, E., Dreyfus, C., Black, I., and Plummer, M. 1995. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA 92(17):8074–8077.

    PubMed  Google Scholar 

  70. Qian, Z., Gilbert, M. E., Colicos, M. A., Kandel, E. R., and Kuhl, D. 1993. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361(6411):453–457.

    PubMed  Google Scholar 

  71. Yamagata, K., Andreasson, K. I., Kaufmann, W. E., Barnes, C.A., and Worley, P. F. 1993. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11(2):371–86.

    PubMed  Google Scholar 

  72. Yamagata, K., Sanders, L. K., Kaufmann, W. E., Yee, W., Barnes, C. A., Nathans, D., and Worley, P. F. 1994. rheb, a growth factor-and synaptic activity-regulated gene, encodes a novel Ras-related protein. J. Biol. Chem. 269(23):16333–16339.

    PubMed  Google Scholar 

  73. Lyford, G. L., Yamagata, K., Kaufmann, W. E., Barnes, C. A., Sanders, L. K., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Lanahan, A. A., and Worley, P. F. 1995. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14(2):433–445.

    PubMed  Google Scholar 

  74. Nedivi, E., Hevroni, D., Naot, D., Israeli, D., and Citri, Y. 1993. Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363:718–721.

    PubMed  Google Scholar 

  75. Naeve, G. S., Ramakrishnan, M., Kramer, R., Hevroni, D., Citri, Y., and Theill, L. E. 1997. Neuritin: a gene induced by neural activity and neurotrophins that promotes neuritogenesis. Proc. Natl. Acad. Sci. USA 94(6):2648–2653.

    PubMed  Google Scholar 

  76. Hevroni, D., Rattner, A., Bundman, M., Lederfein, D., Gabarah, A., Mangelus, M., Silverman, M. A., Kedar, H., Naor, C., Kornuc, M., Hanoch, T., Seger, R., Theill, L. E., Nedivi, E., Richter-Levin, G., and Citri, Y. 1998. Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J. Mol. Neurosci. 10(2):75–98.

    PubMed  Google Scholar 

  77. Adams, M. D., Kelley, J. M., Gocayne, J. D., Dubnick, M., Polymeropoulos, M. H., Xiao, H., Merril, C. R., Wu, A., Olde, B., Moreno, R. F., and et al. 1991. Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252(5013):1651–1656.

    PubMed  Google Scholar 

  78. Adams, M. D., Dubnick, M., Kerlavage, A. R., Moreno, R., Kelley, J. M., Utterback, T. R., Nagle, J. W., Fields, C., and Venter, J. C. 1992. Sequence identification of 2,375 human brain genes. Nature 355(6361):632–634.

    PubMed  Google Scholar 

  79. Sutcliffe, J. G. 2001. Open-system approaches to gene expression in the CNS. J. Neurosci. 21(21):8306–8309.

    PubMed  Google Scholar 

  80. Velculescu, V. E., Zhang, L., Vogelstein, B., and Kinzler, K. W. 1995. Serial analysis of gene expression. Science 270(5235):484–487.

    PubMed  Google Scholar 

  81. Hendriksen, H., Datson, N. A., Ghijsen, W. E., van Vliet, E. A., da Silva, F. H., Gorter, J. A., and Vreugdenhil, E. 2001. Altered hippocampal gene expression prior to the onset of spontaneous seizures in the rat post-status epilepticus model. Eur. J. Neurosci. 14(9):1475–1484.

    PubMed  Google Scholar 

  82. 1999. The Chipping Forecast. Nat. Genet. 21 (Suppl.):1–60.

  83. Sandberg, R., Yasuda, R., Pankratz, D. G., Carter, T. A., Del Rio, J. A., Wodicka, L., Mayford, M., Lockhart, D. J., and Barlow, C. 2000. Regional and strain-specific gene expression mapping in the adult mouse brain. Proc. Natl. Acad. Sci. USA 97(20):11038–11043.

    PubMed  Google Scholar 

  84. Zirlinger, M., Kreiman, G., and Anderson, D. J. 2001. Amygdala-enriched genes identified by microarray technology are restricted to specific amygdaloid subnuclei. Proc. Natl. Acad. Sci. USA 98(9):5270–5275.

    PubMed  Google Scholar 

  85. Zhao, X., Lein, E. S., He, A., Smith, S. C., Aston, C., and Gage, F. H. 2001. Transcriptional profiling reveals strict boundaries between hippocampal subregions. J. Comp. Neurol. 441(3):187–196.

    PubMed  Google Scholar 

  86. Lee, C. K., Klopp, R. G., Weindruch, R., and Prolla, T. A. 1999. Gene expression profile of aging and its retardation by caloric restriction. Science 285(5432):1390–1393.

    PubMed  Google Scholar 

  87. Rampon, C., Jiang, C. H., Dong, H., Tang, Y. P., Lockhart, D. J., Schultz, P. G., Tsien, J. Z., and Hu, Y. 2000. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. USA 97(23):12880–12884.

    PubMed  Google Scholar 

  88. Mody, M., Cao, Y., Cui, Z., Tay, K. Y., Shyong, A., Shimizu, E., Pham, K., Schultz, P., Welsh, D., and Tsien, J. Z. 2001. Genome-wide gene expression profiles of the developing mouse hippocampus. Proc. Natl. Acad. Sci. USA 98(15):8862–8867.

    PubMed  Google Scholar 

  89. Elliott, R. C., Miles, M. F., and Lowenstein, D. H. 2003. Overlapping microarray profiles of dentate gyrus gene expression during development-and epilepsy-associated neurogenesis and axon outgrowth. J. Neurosci. 23(6):2218–2227.

    PubMed  Google Scholar 

  90. Serafini, T. 1999. Of neurons and gene chips. Curr. Opin. Neurobiol. 9(5):641–644.

    PubMed  Google Scholar 

  91. Cao, Y. and Dulac, C. 2001. Profiling brain transcription: neurons learn a lesson from yeast. Curr. Opin. Neurobiol. 11(5):615–620.

    PubMed  Google Scholar 

  92. Lockhart, D. J. and Barlow, C. 2001. Expressing what's on your mind: DNA arrays and the brain. Nat. Rev. Neurosci.2(1):63–68.

    PubMed  Google Scholar 

  93. Amaral, D. G. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182(4 Pt 2):851–914.

    PubMed  Google Scholar 

  94. Freund, T. F. and Buzsaki, G. 1996. Interneurons of the hippocampus. Hippocampus 6(4):347–470.

    PubMed  Google Scholar 

  95. Luo, L., Salunga, R. C., Guo, H., Bittner, A., Joy, K. C., Galindo, J. E., Xiao, H., Rogers, K. E., Wan, J. S., Jackson, M. R., and Erlander, M. G. 1999. Gene expression profiles of laser-captured adjacent neuronal subtypes. Nat. Med. 5(1):117–122.

    PubMed  Google Scholar 

  96. Brady, G. 2000. Expression profiling of single mammalian cells—small is beautiful. Yeast. 17(3):211–217.

    PubMed  Google Scholar 

  97. Eberwine, J., Kacharmina, J. E., Andrews, C., Miyashiro, K., McIntosh, T., Becker, K., Barrett, T., Hinkle, D., Dent, G., and Marciano, P. 2001. mRNA expression analysis of tissue sections and single cells. J. Neurosci. 21(21):8310–8314.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel H. Lowenstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elliott, R.C., Lowenstein, D.H. Gene Expression Profiling of Seizure Disorders. Neurochem Res 29, 1083–1092 (2004). https://doi.org/10.1023/B:NERE.0000023595.12396.1b

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:NERE.0000023595.12396.1b

Navigation