Epigenetic modulation of seizure-induced neurogenesis and cognitive decline

Journal of Neuroscience

Volumn 27, Issue 22, 2007, Pages 5967-5975

  Jessberger, Sebastian ^a   Nakashima, Kinichi ^d   Clemenson Jr , Gregory D ^a   Mejia, Eunice ^a   Mathews, Emily ^a   Ure, Kerstin ^b   Ogawa, Shiori ^c   Sinton, Christopher M ^c   Gage, Fred H ^a   Hsieh, Jenny ^b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Hippocampus; Histone deacetylase; Learning; Neurogenesis; Object recognition; Seizure; Valproic acid

Indexed keywords

HISTONE DEACETYLASE; KAINIC ACID; TRICHOSTATIN A; VALPROIC ACID; VALPROMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DENTATE NUCLEUS; DRUG INDUCED DISEASE; ENZYME INHIBITION; EPIGENETICS; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPORAL LOBE EPILEPSY;

ACTION POTENTIALS; ANIMALS; COGNITION DISORDERS; EPIGENESIS, GENETIC; FEMALE; HIPPOCAMPUS; NEURONS; RATS; RATS, INBRED F344; SEIZURES; VALPROIC ACID;

EID: 34249779216     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0110-07.2007     Document Type: Article

References (73)

1. Ballas N, Battaglioli E, Atouf F, Andres ME, Chenoweth J, Anderson ME, Burger C, Moniwa M, Davie JR, Bowers WJ, Federoff HJ, Rose DW, Rosenfeld MG, Brehm P, Mandel G (2001) Regulation of neuronal traits by a novel transcriptional complex. Neuron 31:353-365.
2. Ben-Ari Y, Cossart R (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23:580-587.
3. Bengzon J, Kokaia Z, Elmér E, Nanobashvili A, Kokaia M, Lindvall O (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 94:10432-10437.
4. Bengzon J, Mohapel P, Ekdahl CT, Lindvall O (2002) Neuronal apoptosis after brief and prolonged seizures. Prog Brain Res 135:111-119.
5. Beuckmann CT, Sinton CM, Williams SC, Richardson JA, Hammer RE, Sakurai T, Yanagisawa M (2004) Expression of a poly-glutamineataxin-3 transgene in orexin neurons induces narcolepsy-cataplexy in the rat. J Neurosci 24:4469-4477.
6. Bolanos AR, Sarkisian M, Yang Y, Hori A, Helmers SL, Mikati M, Tandon P, Stafstrom CE, Holmes GL (1998) Comparison of valproate and phenobarbital treatment after status epilepticus in rats. Neurology 51:41-48.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
8. Buckmaster PS, Dudek FE (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81:712-721.
9. Chong JA, Tapia-Ramirez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80:949-957.
10. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853-8860.
11. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
12. Dashtipour K, Wong AM, Obenaus A, Spigelman I, Ribak CE (2003) Temporal profile of hilar basal dendrite formation on dentate granule cells after status epilepticus. Epilepsy Res 54:141-151.
13. Dupret D, Montaron MF, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2005) Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. Eur J Neurosci 22:778-783.
14. Elger CE, Helmstaedter C, Kurthen M (2004) Chronic epilepsy and cognition. Lancet Neurol 3:663-672.
15. Elliott RC, Miles MF, Lowenstein DH (2003) Overlapping microarray profiles of dentate gyrus gene expression during development- and epilepsy-associated neurogenesis and axon outgrowth. J Neurosci 23:2218-2227.
16. Friedman LK, Pellegrini-Giampietro DE, Sperber EF, Bennett MV, Moshe SL, Zukin RS (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.
17. Gage F (2000) Mammalian neural stem cells. Science 287:1433-1438.
18. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612-613.
19. Gastaldi M, Bartolomei F, Massacrier A, Planells R, Robaglia-Schlupp A, Cau P (1997) Increase in mRNAs encoding neonatal II and III sodium channel alpha-isoforms during kainate-induced seizures in adult rat hippocampus. Brain Res Mol Brain Res 44:179-190.
20. Gerdes J, Schwab U, Lemke H, Stein H (1983) Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31:13-20.
21. Golden GT, Smith GG, Ferraro TN, Reyes PF (1995) Rat strain and age differences in kainic acid induced seizures. Epilepsy Res 20:151-159.
22. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20:6969-6978.
23. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippoampal formation. Nat Neurosci 2:260-265.
24. Grooms SY, Opitz T, Bennett MV, Zukin RS (2000) Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death. Proc Natl Acad Sci USA 97:3631-3636.
25. Gurvich N, Tsygankova OM, Meinkoth JL, Klein PS (2004) Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res 64:1079-1086.
26. Helmstaedter C (2002) Effects of chronic epilepsy on declarative memory systems. Prog Brain Res 135:439-453.
27. Helmstaedter C, Kurthen M, Lux S, Reuber M, Elger CE (2003) Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Ann Neurol 54:425-432.
28. Henry TR (2003) The history of valproate in clinical neuroscience. Psychopharmacol Bull 37 [Suppl 2]:5-16.
29. Holmes GL (1997) Epilepsy in the developing brain: lessons from the laboratory and clinic. Epilepsia 38:12-30.
30. Holtkamp M, Matzen J, van Landeghem F, Buchheim K, Meierkord H (2005) Transient loss of inhibition precedes spontaneous seizures after experimental status epilepticus. Neurobiol Dis 19:162-170.
31. Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 101:16659-16664.
32. Huang Y, Doherty JJ, Dingledine R (2002) Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus. J Neurosci 22:8422-8428.
33. Jakubs K, Nanobashvili A, Bonde S, Ekdahl CT, Kokaia Z, Kokaia M, Lindvall O (2006) Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 52:1047-1059.
34. Jessberger S, Kempermann G (2003) Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18:2707-2712.
35. Jessberger S, Romer B, Babu H, Kempermann G (2005) Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 196:342-351.
36. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
37. Kempermann G (2002) Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
38. Kempermann G, Gage FH (1999) Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 9:321-332.
39. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
40. Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH (2004) A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116:779-793.
41. Majores M, Eils J, Wiestler OD, Becker AJ (2004) Molecular profiling of temporal lobe epilepsy: comparison of data from human tissue samples and animal models. Epilepsy Res 60:173-178.
42. Mohapel P, Ekdahl CT, Lindvall O (2004) Status epilepticus severity influences the long-term outcome of neurogenesis in the adult dentate gyrus. Neurobiol Dis 15:196-205.
43. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955-962.
44. Morland C, Boldingh KA, Iversen EG, Hassel B (2004) Valproate is neuroprotective against malonate toxicity in rat striatum: an association with augmentation of high-affinity glutamate uptake. J Cereb Blood Flow Metab 24:1226-1234.
45. Naruse Y, Aoki T, Kojima T, Mori N (1999) Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuronspecific target genes. Proc Natl Acad Sci USA 96:13691-13696.
46. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL (2006) Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26:4095-4103.
47. Owens MJ, Nemeroff CB (2003) Pharmacology of valproate. Psychopharmacol Bull 37 [Suppl 2]:17-24.
48. Palm K, Belluardo N, Metsis M, Timmusk T (1998) Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J Neurosci 18:1280-1296.
49. Parent JM (2002) The role of seizure-induced neurogenesis in epileptogenesis and brain repair. Epilepsy Res 50:179-189.
50. Parent JM, Lowenstein DH (2002) Seizure-induced neurogenesis: are more new neurons good for an adult brain? Prog Brain Res 135:121-131.
51. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
52. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276:36734-36741.
53. Pollard H, Heron A, Moreau J, Ben-Ari Y, Khrestchatisky M (1993) Alterations of the GluR-B AMPA receptor subunit flip/flop expression in kainate-induced epilepsy and ischemia. Neuroscience 57:545-554.
54. Ren M, Leng Y, Jeong M, Leeds PR, Chuang DM (2004) Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: potential roles of histone deacetylase inhibition and heat shock protein induction. J Neurochem 89:1358-1367.
55. Ribak CE, Tran PH, Spigelman I, Okazaki MM, Nadler JV (2000) Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J Comp Neurol 428:240-253.
56. Sanchez RM, Koh S, Rio C, Wang C, Lamperti ED, Sharma D, Corfas G, Jensen FE (2001) Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21:8154-8163.
57. Scharfman HE, Goodman JH, Sollas AL (2000) Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 20:6144-6158.
58. Schinder AF, Gage FH (2004) A hypothesis about the role of adult neurogenesis in hippocampal function. Physiology (Bethesda) 19:253-261.
59. Schmued LC, Hopkins KJ (2000) Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 28:91-99.
60. Schoenherr CJ, Anderson DJ (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267:1360-1363.
61. Scott BW, Wang S, Burnham WM, De Boni U, Wojtowicz JM (1998) Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci Lett 248:73-76.
62. Shapiro LA, Ribak CE (2006) Newly born dentate granule neurons after pilocarpine-induced epilepsy have hilar basal dendrites with immature synapses. Epilepsy Res 69:53- 66.
63. Shen S, Li J, Casaccia-Bonnefil P (2005) Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J Cell Biol 169:577-589.
64. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
65. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578-584.
66. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843-852.
67. Stafstrom CE, Chronopoulos A, Thurber S, Thompson JL, Holmes GL (1993) Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 34:420-432.
68. Stefan H, Pauli E (2002) Progressive cognitive decline in epilepsy: an indication of ongoing plasticity. Prog Brain Res 135:409-417.
69. Szot P, White SS, Shen DD, Anderson GD (2005) Valproic acid, but not lamotrigine, suppresses seizure-induced c-fos and c-Jun mRNA expression. Brain Res Mol Brain Res 135:285-289.
70. Tongiorgi E, Armellin M, Giulianini PG, Bregola G, Zucchini S, Paradiso B, Steward O, Cattaneo A, Simonato M (2004) Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J Neurosci 24:6842-6852.
71. Van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
72. Winkler I, Blotnik S, Shimshoni J, Yagen B, Devor M, Bialer M (2005) Efficacy of antiepileptic isomers of valproic acid and valpromide in a rat model of neuropathic pain. Br J Pharmacol 146:198-208.
73. Zafra F, Hengerer B, Leibrock J, Thoenen H, Lindholm D (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J 9:3545-3550.